diff --git a/CHANGELOG.md b/CHANGELOG.md
index 6bec8aa28..a7c98a350 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -3,8 +3,16 @@
 
 ## [Unreleased]
 
+### Changed
+
+- **Docs: reconciled the assistant-reply lifecycle RFCs/contracts with shipped behavior.** The Stable Assistant Turn Anchors and Live-to-Final RFCs, `docs/CONTRACTS.md`, and the Phase 0 architecture inventory were updated from "proposed/scaffold" framing to "accepted/implemented" to match what actually ships (single assistant-turn owner projecting one `activity_scene_v1` into Compact Worklog / Transparent Stream / Final answer). Documentation-only — no runtime behavior or CI-gate change; the one code touch is a corrected comment header in `static/assistant_turn_anchors.js`. Remaining hardening stays tracked under #3400. Thanks @franksong2702. (#6144)
+
 ### Fixed
 
+- **Background subagents no longer fail to persist when the parent's cached agent is reused mid-turn.** A parent session's `SessionDB` handle is shared by reference with the background subagents it spawns (`delegate_tool`), but the cached-agent reuse path unconditionally closed that handle when the parent got a new turn / server-side wakeup — so every still-running child then failed `append_message` with `'NoneType' object has no attribute 'execute'` (observed 600+ times under one parent). The reuse path now keeps a still-open handle (closing only the unused fresh one, preserving the #1421 FD-leak fix) and only replaces a dead/missing one. The credential self-heal path was hardened the same way: if rebuilding the handle fails it degrades cleanly to a lazy reinit instead of reusing a closed handle. Thanks @carlotestor. (#6143)
+
+- **The CLI/cron session-list projection cache is now bounded.** `_CLI_SESSIONS_CACHE` was an unbounded plain dict of deep-copied session-list projections whose fingerprint-folded key advances on every streamed message, so orphaned heavy copies accumulated on a long-lived server until the next structural clear. It's now an `OrderedDict` capped at 8 entries with drop-oldest LRU eviction (recency refresh on hit), mirroring the existing `_CLAUDE_CODE_PARSE_CACHE` / `_SIDECAR_METADATA_CACHE` pattern; TTL stays the freshness control. Thanks @rh-id. (#6140)
+
 - **Models selected from a list-shaped custom-provider allowlist now route to the right provider.** A `custom_providers[].models` allowlist can be written as either a mapping or a list, and the model picker accepted both — but runtime routing only read mapping keys, so a model chosen from a *list*-shaped allowlist could silently stay on the active/default provider instead of its own. The supported-model-ID extraction is now centralized in one helper used by both catalog construction and routing, so the picker and runtime can no longer drift. Existing mapping-shaped and list-of-strings configs are unaffected. Thanks @franksong2702. (#6127, #6121)
 
 - **Stale sidebar approval attention badge now clears once its gateway approval has drained.** A parent session could keep showing the red approval "attention" dot in the sidebar after the underlying gateway approval was already resolved/gone — the live gateway queue drained but the sidebar summary kept the mirrored approval alive. `_session_attention_summary()` now reconciles the gateway pending-mirror before counting attention (the same self-healing repair the approval-pending route already does), so the badge clears correctly. Live approvals stay visible and actionable and the clarify fallback is unchanged. This is the WebUI read-path mitigation; the child-session context-propagation root cause stays tracked in #6100. Thanks @rodboev. (#6117, #6100)
diff --git a/api/agent_runtime.py b/api/agent_runtime.py
new file mode 100644
index 000000000..865a2fd50
--- /dev/null
+++ b/api/agent_runtime.py
@@ -0,0 +1,163 @@
+"""Fail-closed guard for in-process Hermes Agent source revisions.
+
+Hermes WebUI currently imports ``run_agent.AIAgent`` into its long-lived server
+process. If the Agent checkout changes while that process is alive, Python may
+combine already-cached modules with newly-read source. Refuse to reuse that
+mixed runtime and require a clean WebUI restart instead.
+"""
+
+from __future__ import annotations
+
+from pathlib import Path
+import sys
+import subprocess
+import threading
+
+# Retain the discovered path as a diagnostic/test-visible compatibility value;
+# runtime identity is deliberately captured from the loaded module below.
+from api.config import _AGENT_DIR  # noqa: F401
+
+_RESTART_MESSAGE = (
+    "Hermes Agent was updated while Hermes WebUI was running. "
+    "Restart Hermes WebUI before retrying this action."
+)
+
+
+def _read_agent_revision(
+    agent_dir: Path | None,
+    *,
+    module_path: Path | None = None,
+) -> str | None:
+    """Return the loaded Agent checkout HEAD, or ``None`` if it is not tracked."""
+    if agent_dir is None:
+        return None
+
+    if module_path is None:
+        module = sys.modules.get("run_agent")
+        module_file = getattr(module, "__file__", None)
+        if not module_file:
+            return None
+        try:
+            module_path = Path(module_file).resolve()
+        except (OSError, RuntimeError, TypeError):
+            return None
+
+    try:
+        worktree_result = subprocess.run(
+            ["git", "-C", str(agent_dir), "rev-parse", "--show-toplevel"],
+            check=False,
+            capture_output=True,
+            text=True,
+            timeout=2,
+        )
+        if worktree_result.returncode != 0:
+            return None
+        worktree = Path(worktree_result.stdout.strip()).resolve()
+        relative_module = module_path.relative_to(worktree).as_posix()
+        tracked_result = subprocess.run(
+            [
+                "git",
+                "--literal-pathspecs",
+                "-C",
+                str(worktree),
+                "ls-files",
+                "--error-unmatch",
+                "--",
+                relative_module,
+            ],
+            check=False,
+            capture_output=True,
+            text=True,
+            timeout=2,
+        )
+        if tracked_result.returncode != 0:
+            return None
+        revision_result = subprocess.run(
+            ["git", "-C", str(worktree), "rev-parse", "--verify", "HEAD"],
+            check=False,
+            capture_output=True,
+            text=True,
+            timeout=2,
+        )
+    except (OSError, subprocess.TimeoutExpired, RuntimeError, ValueError):
+        return None
+
+    revision = revision_result.stdout.strip()
+    return revision if revision_result.returncode == 0 and revision else None
+
+
+_AGENT_SOURCE_DIR: Path | None = None
+_AGENT_MODULE_PATH: Path | None = None
+_AGENT_REVISION: str | None = None
+_AIAgent = None
+_RUNTIME_LOCK = threading.Lock()
+
+
+class AgentRuntimeChangedError(RuntimeError):
+    """Raised when the loaded Agent runtime no longer matches its source tree."""
+
+
+def _loaded_agent_source_identity() -> tuple[Path, Path] | None:
+    """Return the source directory and file that supplied ``run_agent``."""
+    module = sys.modules.get("run_agent")
+    module_file = getattr(module, "__file__", None)
+    if not module_file:
+        return None
+    try:
+        module_path = Path(module_file).resolve()
+        return module_path.parent, module_path
+    except (OSError, RuntimeError, TypeError):
+        return None
+
+
+def _capture_loaded_agent_revision() -> None:
+    """Bind the guard to the checkout that supplied the loaded Agent module."""
+    global _AGENT_SOURCE_DIR, _AGENT_MODULE_PATH, _AGENT_REVISION
+
+    if _AGENT_REVISION is not None:
+        ensure_agent_runtime_current()
+        return
+
+    identity = _loaded_agent_source_identity()
+    if identity is None:
+        return
+    source_dir, module_path = identity
+    current_revision = _read_agent_revision(source_dir, module_path=module_path)
+    _AGENT_SOURCE_DIR = source_dir
+    _AGENT_MODULE_PATH = module_path
+    _AGENT_REVISION = current_revision
+
+
+def ensure_agent_runtime_current() -> None:
+    """Reject a known Git checkout change instead of mixing Python modules."""
+    if _AGENT_REVISION is None:
+        return
+    if (
+        _read_agent_revision(_AGENT_SOURCE_DIR, module_path=_AGENT_MODULE_PATH)
+        != _AGENT_REVISION
+    ):
+        raise AgentRuntimeChangedError(_RESTART_MESSAGE)
+
+
+def require_ai_agent_class():
+    """Import ``AIAgent`` after proving the loaded source revision is current."""
+    ensure_agent_runtime_current()
+    from run_agent import AIAgent  # noqa: PLC0415
+
+    _capture_loaded_agent_revision()
+    return AIAgent
+
+
+def get_ai_agent_class():
+    """Return ``AIAgent`` while preserving the existing lazy-import retry."""
+    global _AIAgent, _AGENT_REVISION
+
+    with _RUNTIME_LOCK:
+        ensure_agent_runtime_current()
+        if _AIAgent is None:
+            try:
+                agent_class = require_ai_agent_class()
+            except ImportError:
+                return None
+            _AIAgent = agent_class
+        return _AIAgent
diff --git a/api/models.py b/api/models.py
index 48a879a11..49888ad2f 100644
--- a/api/models.py
+++ b/api/models.py
@@ -63,7 +63,16 @@ _CLI_SESSIONS_CACHE_STREAMING_TTL_SECONDS = 45.0
 _CLI_SESSIONS_CACHE_LOCK = threading.Lock()
 _CLI_SESSIONS_CACHE_INFLIGHT: "dict[tuple, threading.Event]" = {}
 _CLI_SESSIONS_CACHE_INVALIDATION_VERSION = 0
-_CLI_SESSIONS_CACHE = {}
+# LRU-bounded (drop-oldest) so a long-lived process under churn — where the
+# state.db fingerprint advances on every streamed message and the structural
+# clear-on-mutation listener doesn't fire for every fingerprint advance — can't
+# accumulate orphaned heavy deepcopies. Each value is a copy.deepcopy() of the
+# full CLI/cron session list (the expensive projection behind #4842/#4672), so
+# the cap is deliberately small. TTL is still the primary freshness control;
+# the cap is the backstop that the plain dict previously lacked. Mirrors the
+# _CLAUDE_CODE_PARSE_CACHE / _SIDECAR_METADATA_CACHE LRU pattern.
+_CLI_SESSIONS_CACHE: "collections.OrderedDict[tuple, tuple]" = collections.OrderedDict()
+_CLI_SESSIONS_CACHE_MAX_ENTRIES = 8
 _CLI_SESSIONS_CACHE_WAIT_SECONDS = 0.25
 # Event waits that keep stale rows visible while a rebuild is in flight.
 _CLI_SESSIONS_CACHE_STALE_WAIT_SECONDS = 0.10
@@ -6405,6 +6414,9 @@ def _cache_cli_sessions_if_current(
             invalidation_stamp,
             _copy_cli_sessions(sessions),
         )
+        _CLI_SESSIONS_CACHE.move_to_end(cache_key)
+        while len(_CLI_SESSIONS_CACHE) > _CLI_SESSIONS_CACHE_MAX_ENTRIES:
+            _CLI_SESSIONS_CACHE.popitem(last=False)
     return True
 
 
@@ -6423,6 +6435,8 @@ def _copy_fresh_cli_sessions_cache_entry(cache_key: tuple):
             return None
         if cached_expires_at <= time.monotonic():
             return None
+        # LRU: a fresh hit is the most-recently-used entry.
+        _CLI_SESSIONS_CACHE.move_to_end(cache_key)
         return _copy_cli_sessions(cached_sessions)
 
 
@@ -7272,6 +7286,8 @@ def get_cli_sessions(
                 if cached_stamp != _CLI_SESSIONS_CACHE_INVALIDATION_VERSION:
                     _CLI_SESSIONS_CACHE.pop(cache_key, None)
                 elif cached_expires_at > now:
+                    # LRU: a fresh hit is the most-recently-used entry.
+                    _CLI_SESSIONS_CACHE.move_to_end(cache_key)
                     return _copy_cli_sessions(cached_sessions)
                 else:
                     stale_sessions = _copy_cli_sessions(cached_sessions)
diff --git a/api/routes.py b/api/routes.py
index 2a654ab5a..58b93f6e7 100644
--- a/api/routes.py
+++ b/api/routes.py
@@ -34,6 +34,11 @@ from contextlib import closing
 from urllib.parse import parse_qs, quote, unquote, urljoin, urlsplit
 from urllib.error import HTTPError, URLError
 from urllib.request import HTTPRedirectHandler, HTTPSHandler, ProxyHandler, Request, build_opener
+from api.agent_runtime import (
+    AgentRuntimeChangedError,
+    ensure_agent_runtime_current,
+    require_ai_agent_class,
+)
 from api.agent_sessions import (
     MESSAGING_SOURCES,
     _looks_like_default_cli_title,
@@ -16052,6 +16057,7 @@ def handle_post(handler, parsed) -> bool:
                     "api_key": _main_api_key,
                 }
 
+                ensure_agent_runtime_current()
                 try:
                     from agent.auxiliary_client import get_text_auxiliary_client
 
@@ -16072,7 +16078,7 @@ def handle_post(handler, parsed) -> bool:
                 except Exception as _e:
                     logger.debug("update summary auxiliary model failed; falling back to main model: %s", _e)
 
-                from run_agent import AIAgent
+                AIAgent = require_ai_agent_class()
 
                 agent = AIAgent(
                     model=_main_model,
@@ -20425,6 +20431,9 @@ def _handle_btw(handler, body):
         require(body, "question")
     except ValueError as e:
         return bad(handler, str(e))
+    stale_response = _agent_runtime_barrier_response(runner_local_owned=False)
+    if stale_response is not None:
+        return j(handler, stale_response, status=409)
     if _session_is_subagent_view_only(str(body.get("session_id") or "")):
         return bad(handler, "Subagent sessions are view-only and cannot be used for /btw from WebUI", 400)
     try:
@@ -20484,6 +20493,9 @@ def _handle_background(handler, body):
         require(body, "prompt")
     except ValueError as e:
         return bad(handler, str(e))
+    stale_response = _agent_runtime_barrier_response(runner_local_owned=False)
+    if stale_response is not None:
+        return j(handler, stale_response, status=409)
     try:
         s = get_session(body["session_id"])
     except KeyError:
@@ -20770,6 +20782,31 @@ def _active_run_stream_for_session(session_id: str | None) -> str | None:
     return None
 
 
+def _agent_runtime_barrier_response(
+    *,
+    runner_local_owned: bool = False,
+    external_runtime_owned: bool | None = None,
+) -> dict | None:
+    """Return the typed stale-runtime response for local in-process turns."""
+    if external_runtime_owned is True:
+        return None
+    if runner_local_owned and webui_gateway_chat_enabled(get_config()):
+        return None
+    from api.runtime_adapter import runtime_adapter_runner_enabled
+
+    if runner_local_owned and runtime_adapter_runner_enabled():
+        return None
+    try:
+        ensure_agent_runtime_current()
+    except AgentRuntimeChangedError as exc:
+        return {
+            "error": str(exc),
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        }
+    return None
+
+
 def _start_chat_stream_for_session(
     s,
     *,
@@ -20783,8 +20820,18 @@ def _start_chat_stream_for_session(
     goal_related: bool = False,
     source: str = "webui",
     moa_config=None,
+    external_runtime_owned: bool | None = None,
 ):
     """Persist pending state, register an SSE channel, and start an agent turn."""
+    if external_runtime_owned is None:
+        external_runtime_owned = webui_gateway_chat_enabled(get_config())
+    backend_is_gateway = bool(external_runtime_owned)
+    stale_response = _agent_runtime_barrier_response(
+        external_runtime_owned=backend_is_gateway,
+    )
+    if stale_response is not None:
+        stale_response["_status"] = 409
+        return stale_response
     attachments = attachments or []
     # Prevent duplicate runs in the same session while a stream is still active.
     # This commonly happens after page refresh/reconnect races and can produce
@@ -20903,7 +20950,6 @@ def _start_chat_stream_for_session(
     if goal_related:
         STREAM_GOAL_RELATED[stream_id] = True
     diag.stage("worker_thread_start") if diag else None
-    backend_is_gateway = webui_gateway_chat_enabled(get_config())
     worker_target = _run_gateway_chat_streaming if backend_is_gateway else _run_agent_streaming
     worker_kwargs = {"model_provider": model_provider, "goal_related": goal_related}
     if moa_config and not backend_is_gateway:
@@ -21074,6 +21120,7 @@ def _start_run(
         diag=diag,
         source=source,
         moa_config=moa_config,
+        external_runtime_owned=webui_gateway_chat_enabled(get_config()),
     )
 
 
@@ -21167,6 +21214,10 @@ def start_session_turn(
     msg = str(message or "").strip()
     if not msg:
         return {"error": "message is required", "_status": 400}
+    stale_response = _agent_runtime_barrier_response(runner_local_owned=True)
+    if stale_response is not None:
+        stale_response["_status"] = 409
+        return stale_response
     turn_source = str(source or "process_wakeup").strip() or "process_wakeup"
     try:
         s = get_session(session_id)
@@ -21643,6 +21694,7 @@ def _handle_goal_command(handler, body):
             model_provider=model_provider,
             normalized_model=normalized_model,
             goal_related=True,
+            external_runtime_owned=webui_gateway_chat_enabled(get_config()),
         )
         status = int(stream_response.pop("_status", 200) or 200)
         payload.update(stream_response)
@@ -21661,6 +21713,12 @@ def _handle_chat_start(handler, body, diag=None):
             require(body, "session_id")
         except ValueError as e:
             return bad(handler, str(e))
+        # Reject a stale local Agent runtime before materialising, claiming, or
+        # mutating any session state. Gateway-backed turns run in the gateway's
+        # process and do not depend on this WebUI process's imported checkout.
+        stale_response = _agent_runtime_barrier_response(runner_local_owned=True)
+        if stale_response is not None:
+            return j(handler, stale_response, status=409)
         diag.stage("get_session") if diag else None
         try:
             s = _get_or_materialize_session(body["session_id"], refresh_cli_messages=True)
@@ -21956,6 +22014,9 @@ def _normalize_chat_attachments(raw_attachments):
 
 def _handle_chat_sync(handler, body):
     """Fallback synchronous chat endpoint (POST /api/chat). Not used by frontend."""
+    stale_response = _agent_runtime_barrier_response(runner_local_owned=False)
+    if stale_response is not None:
+        return j(handler, stale_response, status=409)
     if _session_is_subagent_view_only(str(body.get("session_id") or "")):
         return bad(handler, "Subagent sessions are view-only and cannot be written from WebUI", 400)
     s = get_session(body["session_id"])
@@ -21991,7 +22052,7 @@ def _handle_chat_sync(handler, body):
         os.environ["HERMES_EXEC_ASK"] = "1"
         os.environ["HERMES_SESSION_KEY"] = s.session_id
     try:
-        from run_agent import AIAgent
+        AIAgent = require_ai_agent_class()
 
         with CHAT_LOCK:
             from api.config import (
@@ -22622,6 +22683,7 @@ def _llm_git_commit_message(system_prompt: str, user_prompt: str, session=None)
             "base_url": _main_base_url,
             "api_key": _main_api_key,
         }
+        ensure_agent_runtime_current()
         try:
             from agent.auxiliary_client import get_text_auxiliary_client
 
@@ -22638,7 +22700,7 @@ def _llm_git_commit_message(system_prompt: str, user_prompt: str, session=None)
         except Exception as _e:
             logger.debug("git commit message auxiliary model failed; falling back to main model: %s", _e)
 
-        from run_agent import AIAgent
+        AIAgent = require_ai_agent_class()
 
         agent = AIAgent(
             model=_main_model,
@@ -22684,6 +22746,12 @@ def _handle_git_commit_message(handler, body):
         return bad(handler, str(e))
     except GitWorkspaceError as e:
         return _git_bad(handler, e)
+    except AgentRuntimeChangedError as e:
+        return j(handler, {
+            "error": str(e),
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        }, status=409)
     except Exception as e:
         logger.exception("git commit message generation failed")
         return bad(handler, _sanitize_error(e), 500)
@@ -22715,6 +22783,12 @@ def _handle_git_commit_message_selected(handler, body):
         return bad(handler, str(e))
     except GitWorkspaceError as e:
         return _git_bad(handler, e)
+    except AgentRuntimeChangedError as e:
+        return j(handler, {
+            "error": str(e),
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        }, status=409)
     except Exception as e:
         logger.exception("selected git commit message generation failed")
         return bad(handler, _sanitize_error(e), 500)
@@ -23739,6 +23813,10 @@ def _manual_compression_status_payload(job):
         payload["ok"] = False
         payload["error"] = job.get("error") or "Compression failed"
         payload["error_status"] = int(job.get("error_status") or 400)
+        if job.get("error_type"):
+            payload["type"] = job["error_type"]
+        if job.get("retryable") is not None:
+            payload["retryable"] = bool(job["retryable"])
     elif status == "cancelled":
         payload["ok"] = False
         payload["error"] = job.get("error") or "Compression cancelled"
@@ -23773,6 +23851,8 @@ def _run_manual_compression_job(sid, body):
                         "status": "error",
                         "error": str((payload or {}).get("error") or "Compression failed"),
                         "error_status": status,
+                        "error_type": (payload or {}).get("type"),
+                        "retryable": (payload or {}).get("retryable"),
                         "updated_at": now,
                     }
                 )
@@ -23784,6 +23864,21 @@ def _run_manual_compression_job(sid, body):
                         "updated_at": now,
                     }
                 )
+    except AgentRuntimeChangedError as exc:
+        logger.warning("Manual compression worker found stale Agent runtime for session %s", sid)
+        with _MANUAL_COMPRESSION_JOBS_LOCK:
+            job = _MANUAL_COMPRESSION_JOBS.get(sid)
+            if job:
+                job.update(
+                    {
+                        "status": "error",
+                        "error": str(exc),
+                        "error_status": 409,
+                        "error_type": "agent_runtime_stale",
+                        "retryable": True,
+                        "updated_at": time.time(),
+                    }
+                )
     except Exception as exc:
         logger.warning("Manual compression worker failed for session %s: %s", sid, exc)
         with _MANUAL_COMPRESSION_JOBS_LOCK:
@@ -23820,6 +23915,34 @@ def _handle_session_compress_start(handler, body):
     if focus_topic:
         job_body["focus_topic"] = focus_topic
 
+    # Repeated start requests observe an existing running job and do not admit
+    # new Agent work, so preserve that idempotent read even if the checkout has
+    # since changed. Do not hold the job lock while running Git subprocesses.
+    now = time.time()
+    with _MANUAL_COMPRESSION_JOBS_LOCK:
+        _manual_compression_cleanup_locked(now)
+        existing = _MANUAL_COMPRESSION_JOBS.get(sid)
+        if existing:
+            existing_payload = _manual_compression_status_payload(existing)
+            if existing_payload.get("status") == "running":
+                return j(handler, existing_payload)
+
+    # Reject a stale local Agent runtime before creating the asynchronous job.
+    try:
+        ensure_agent_runtime_current()
+    except AgentRuntimeChangedError as exc:
+        return j(
+            handler,
+            {
+                "error": str(exc),
+                "type": "agent_runtime_stale",
+                "retryable": True,
+            },
+            status=409,
+        )
+
+    # Another start request may have admitted a job while the runtime check ran.
+    # Re-check under the lock so only one worker is created.
     now = time.time()
     with _MANUAL_COMPRESSION_JOBS_LOCK:
         _manual_compression_cleanup_locked(now)
@@ -24035,10 +24158,11 @@ def _handle_session_compress(handler, body):
                     focus_topic,
                 )
 
+        ensure_agent_runtime_current()
         import api.config as _cfg
         from api.oauth import resolve_runtime_provider_with_anthropic_env_lock
         import hermes_cli.runtime_provider as _runtime_provider
-        import run_agent as _run_agent
+        AIAgent = require_ai_agent_class()
 
         resolved_model, resolved_provider, resolved_base_url = _cfg.resolve_model_provider(
             _cfg.model_with_provider_context(s.model, getattr(s, "model_provider", None))
@@ -24081,7 +24205,7 @@ def _handle_session_compress(handler, body):
         )
         approx_tokens = _estimate_messages_tokens_rough(original_messages)
 
-        agent = _run_agent.AIAgent(
+        agent = AIAgent(
             model=resolved_model,
             provider=resolved_provider,
             base_url=resolved_base_url,
@@ -24176,6 +24300,12 @@ def _handle_session_compress(handler, body):
                 "focus_topic": focus_topic,
             },
         )
+    except AgentRuntimeChangedError as e:
+        return j(handler, {
+            "error": str(e),
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        }, status=409)
     except Exception as e:
         logger.warning("Manual session compression failed: %s", e)
         return bad(handler, f"Compression failed: {_sanitize_error(e)}")
@@ -24685,10 +24815,11 @@ def _handle_handoff_summary(handler, body):
 
         # Call LLM for summary.
     try:
+        ensure_agent_runtime_current()
         import api.config as _cfg
         from api.oauth import resolve_runtime_provider_with_anthropic_env_lock
         import hermes_cli.runtime_provider as _runtime_provider
-        import run_agent as _run_agent
+        AIAgent = require_ai_agent_class()
 
         # Try to resolve model from an existing session, fall back to default.
         resolved_model = None
@@ -24744,7 +24875,7 @@ def _handle_handoff_summary(handler, body):
                 "fallback": True,
             })
 
-        agent = _run_agent.AIAgent(
+        agent = AIAgent(
             model=resolved_model,
             provider=resolved_provider,
             base_url=resolved_base_url,
@@ -24824,6 +24955,12 @@ def _handle_handoff_summary(handler, body):
             "rounds": rounds,
             "fallback": fallback,
         })
+    except AgentRuntimeChangedError as e:
+        return j(handler, {
+            "error": str(e),
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        }, status=409)
     except Exception as e:
         logger.warning("Handoff summary generation failed: %s", e)
         summary_text = _fallback_handoff_summary(msgs)
diff --git a/api/streaming.py b/api/streaming.py
index c733a8f9a..7ef3dd998 100644
--- a/api/streaming.py
+++ b/api/streaming.py
@@ -564,10 +564,13 @@ def _prewarm_skill_tool_modules():
 
 
 # Lazy import to avoid circular deps -- hermes-agent is on sys.path via api/config.py
-try:
-    from run_agent import AIAgent
-except ImportError:
-    AIAgent = None
+from api.agent_runtime import ensure_agent_runtime_current, get_ai_agent_class
+
+
+# Eagerly attempt the import at startup, matching the pre-guard behavior. If
+# dependencies are not ready yet, _get_ai_agent() retries when a chat starts.
+AIAgent = get_ai_agent_class()
+
 
 def _get_ai_agent():
     """Return AIAgent class, retrying the import if the initial attempt failed.
@@ -575,15 +578,13 @@ def _get_ai_agent():
     auto_install_agent_deps() in server.py may install missing packages after
     this module is first imported (common in Docker with a volume-mounted agent).
     Re-attempting the import here picks up the newly installed packages without
-    requiring a server restart.
+    requiring a server restart. The shared runtime guard also refuses to reuse
+    cached Agent modules after the source checkout changes.
     """
     global AIAgent
+    ensure_agent_runtime_current()
     if AIAgent is None:
-        try:
-            from run_agent import AIAgent as _cls  # noqa: PLC0415
-            AIAgent = _cls
-        except ImportError:
-            pass
+        AIAgent = get_ai_agent_class()
     return AIAgent
 
 
@@ -6265,6 +6266,65 @@ def _last_resort_sync_from_core(session, stream_id, agent_lock):
         )
 
 
+def _session_db_is_open(session_db) -> bool:
+    """True when *session_db* still has a live sqlite connection.
+
+    SessionDB.close() sets ``_conn = None``. Subagents capture the parent's
+    SessionDB object by reference at spawn time (delegate_tool), so closing
+    that object mid-parent-turn makes every subsequent child
+    ``append_message`` fail with
+    ``'NoneType' object has no attribute 'execute'``.
+    """
+    if session_db is None:
+        return False
+    return getattr(session_db, "_conn", None) is not None
+
+
+def _adopt_session_db_for_cached_agent(agent, new_session_db):
+    """Attach a SessionDB to a reused cached agent without breaking subagents.
+
+    Historical behaviour (PR #1421 FD-leak fix): create a fresh SessionDB every
+    stream request and close the previous handle before replacing
+    ``agent._session_db``. That stops EMFILE growth, but a server-side wakeup
+    / new turn for the same parent session will close the shared handle while
+    background subagents are still writing into it.
+
+    Policy now:
+    - If the cached agent already holds an *open* SessionDB, keep it and close
+      the unused new handle (no FD leak; live subagents keep working).
+    - If the existing handle is missing or already closed, adopt *new_session_db*.
+    - If *new_session_db* is None, leave the existing handle alone.
+    """
+    if agent is None:
+        return new_session_db
+    existing = getattr(agent, "_session_db", None)
+    if new_session_db is None:
+        return existing
+    if existing is new_session_db:
+        return existing
+    if _session_db_is_open(existing):
+        try:
+            new_session_db.close()
+        except Exception:
+            # Same observability as _replace_session_db_in_kwargs: a failed
+            # close here reintroduces the EMFILE pressure PR #1421 fixed.
+            logger.debug(
+                "Failed to close unused session_db handle in adopt helper",
+                exc_info=True,
+            )
+        return existing
+    if existing is not None:
+        try:
+            existing.close()
+        except Exception:
+            logger.debug(
+                "Failed to close previous session_db handle in adopt helper",
+                exc_info=True,
+            )
+    agent._session_db = new_session_db
+    return new_session_db
+
+
 def _build_session_db_for_stream(state_db_path):
     """Build a per-request SessionDB handle for WebUI session search.
 
@@ -6280,12 +6340,36 @@ def _build_session_db_for_stream(state_db_path):
 
 
 def _replace_session_db_in_kwargs(agent_kwargs, state_db_path):
-    """Build a fresh SessionDB and replace ``agent_kwargs['session_db']`` safely."""
+    """Build a fresh SessionDB and replace ``agent_kwargs['session_db']`` safely.
+
+    Does not close an existing open handle that may still be shared with live
+    subagents; only replaces when the prior handle is missing or already closed.
+    """
     if not isinstance(agent_kwargs, dict):
         return None
 
     _old_session_db = agent_kwargs.get("session_db")
     _next_session_db = _build_session_db_for_stream(state_db_path)
+    if _next_session_db is None:
+        # Replacement construction failed. Keep the prior handle only if it is
+        # still open (live subagents may hold it by reference); otherwise
+        # degrade cleanly to None — as master did — so the rebuilt agent lazily
+        # reinitialises its SessionDB instead of reusing a closed handle and
+        # failing every persist/search with
+        # "'NoneType' object has no attribute 'execute'".
+        if _session_db_is_open(_old_session_db):
+            return _old_session_db
+        agent_kwargs["session_db"] = None
+        return None
+    if _session_db_is_open(_old_session_db):
+        # Keep the live handle; discard the unused new one.
+        try:
+            if _next_session_db is not _old_session_db:
+                _next_session_db.close()
+        except Exception:
+            logger.debug("Failed to close unused session_db handle during self-heal")
+        agent_kwargs["session_db"] = _old_session_db
+        return _old_session_db
     if _old_session_db is not None and _old_session_db is not _next_session_db:
         try:
             _old_session_db.close()
@@ -7213,6 +7297,7 @@ def _run_agent_streaming(
             logger.debug("register_process_session failed", exc_info=True)
         # first-time module initialisation (which can be slow) does not
         # block other concurrent sessions waiting on _ENV_LOCK (#2024).
+        ensure_agent_runtime_current()
         _prewarm_skill_tool_modules()
         _install_streaming_cronjob_profile_wrapper()
         # Still set process-level env as fallback for tools that bypass thread-local
@@ -8295,15 +8380,19 @@ def _run_agent_streaming(
                     if 'prefill_messages' in _agent_kwargs and hasattr(agent, 'prefill_messages'):
                         agent.prefill_messages = list(_agent_kwargs.get('prefill_messages') or [])
                     if _session_db is not None:
-                        # Close any previously held SessionDB connection before
-                        # replacing it. Without this, each streaming request creates
-                        # a new SessionDB whose WAL handles leak indefinitely,
-                        # eventually causing EMFILE crashes (#streaming FD leak).
-                        if hasattr(agent, '_session_db') and agent._session_db is not None:
-                            try:
-                                agent._session_db.close()
-                            except Exception:
-                                pass
+                        # Prefer reusing a still-open SessionDB on the cached
+                        # agent. Closing it mid-turn breaks background
+                        # subagents that hold a reference to the same object
+                        # (delegate_tool copies parent._session_db by ref) —
+                        # they then fail with
+                        # 'NoneType' object has no attribute 'execute'.
+                        # When the existing handle is already closed/missing,
+                        # adopt the fresh per-request SessionDB (and close the
+                        # dead one) so we still avoid the EMFILE FD-leak from
+                        # PR #1421.
+                        _session_db = _adopt_session_db_for_cached_agent(
+                            agent, _session_db
+                        )
                         agent._session_db = _session_db
                     if hasattr(agent, '_api_call_count'):
                         agent._api_call_count = 0
diff --git a/docs/CONTRACTS.md b/docs/CONTRACTS.md
index 0094a5c28..e7bcc6fc3 100644
--- a/docs/CONTRACTS.md
+++ b/docs/CONTRACTS.md
@@ -29,13 +29,19 @@ contributor guidance; it does not change runtime behavior or CI gates.
   repairs. Start here for narrow fixes that keep the existing WebUI execution
   path.
 - [`docs/rfcs/live-to-final-assistant-replies.md`](rfcs/live-to-final-assistant-replies.md):
-  proposed product model for long-running assistant replies, live process text,
+  accepted product model for long-running assistant replies, live process text,
   tool activity, recovery, terminal outcomes, and final-answer boundaries. Start
   here for UI/UX changes to running-session assistant reply rendering.
+- [`docs/rfcs/stable-assistant-turn-anchors.md`](rfcs/stable-assistant-turn-anchors.md):
+  implemented presentation/reconciliation model that attaches live, settled,
+  replayed, and recovered activity to one assistant-turn owner and projects one
+  `activity_scene_v1` into Compact Worklog, Transparent Stream, or Final answer
+  only. Remaining hardening stays tracked under #3400.
 - [`docs/architecture/stable-assistant-turn-anchor-phase0.md`](architecture/stable-assistant-turn-anchor-phase0.md):
-  current Phase 0 inventory for the Stable Assistant Turn Anchors work under
-  #3926. Use this before wiring anchor helpers into live SSE, replay,
-  settlement, `INFLIGHT`, or `renderMessages()` paths.
+  cumulative implementation inventory for the Stable Assistant Turn Anchors
+  work under #3926. Use it to distinguish shipped wiring from historical slice
+  boundaries before changing live SSE, replay, settlement, `INFLIGHT`, or
+  `renderMessages()` paths.
 - [`docs/rfcs/canonical-session-resolution.md`](rfcs/canonical-session-resolution.md):
   proposed contract for resolving URL routes, query parameters, localStorage,
   sidebar rows, and compression-lineage IDs to one canonical visible session
diff --git a/docs/architecture/stable-assistant-turn-anchor-phase0.md b/docs/architecture/stable-assistant-turn-anchor-phase0.md
index b09ef65ae..ceea20232 100644
--- a/docs/architecture/stable-assistant-turn-anchor-phase0.md
+++ b/docs/architecture/stable-assistant-turn-anchor-phase0.md
@@ -1,12 +1,16 @@
 # Stable Assistant Turn Anchors Phase 0 Inventory
 
-This inventory implements the first non-visual slice of
-[`stable-assistant-turn-anchors.md`](../rfcs/stable-assistant-turn-anchors.md).
-It documents the current per-turn state layers and the event-shape contract that
-future anchor phases must consume. It does not claim that anchors are wired into
-streaming or rendering yet.
+This inventory began as the first non-visual slice of
+[`stable-assistant-turn-anchors.md`](../rfcs/stable-assistant-turn-anchors.md) and
+now records the shipped phase progression. Current `master` wires Anchor-owned
+`activity_scene_v1` data into live and settled Compact Worklog, Transparent
+Stream, journal hydration, session re-entry, and transcript-backed persistence.
 
-## RFC Phase Progress
+The slice-by-slice sections below are retained as implementation history.
+Present-tense statements such as “unwired” or “future phase” describe the point
+when that slice landed; they do not override the current coverage summary above.
+
+## Shipped RFC Phase Progress
 
 - The #3962 Phase 0 scaffold shipped through #3977 / v0.51.359: inventory the
   current state layers, encode the owner seed, and pin the source classification
diff --git a/docs/rfcs/README.md b/docs/rfcs/README.md
index 921bb2d45..d728461d1 100644
--- a/docs/rfcs/README.md
+++ b/docs/rfcs/README.md
@@ -47,16 +47,17 @@ First-time contributor RFCs should be discussed in an issue before opening a PR.
   replay, compression, and session metadata coherent during active and recovered
   WebUI runs.
 - [`live-to-final-assistant-replies.md`](live-to-final-assistant-replies.md)
-  — #3400 product model for long-running assistant replies, live process prose,
-  tool activity, recovery, terminal outcomes, and the final-answer boundary.
+  — #3400 accepted product model for long-running assistant replies, live
+  process prose, tool activity, recovery, terminal outcomes, display
+  projections, and the final-answer boundary.
 - [`transparent-stream-activity-mode.md`](transparent-stream-activity-mode.md)
-  — #3820 opt-in display mode for power users who need a transparent,
-  chronological Thinking / progress / tool-call stream alongside the default
-  Compact Worklog model.
+  — #3820 implemented opt-in display mode for power users who need a
+  transparent, chronological Thinking / progress / tool-call stream alongside
+  the default Compact Worklog and opt-in Final answer only projections.
 - [`stable-assistant-turn-anchors.md`](stable-assistant-turn-anchors.md) — #3926
-  proposed frontend presentation/reconciliation model for anchoring live
-  assistant activity, settled final answers, replay, and Compact/Transparent
-  render modes to one assistant turn.
+  implemented frontend presentation/reconciliation model for anchoring live
+  assistant activity, settled final answers, replay, and all activity display
+  modes to one assistant turn; remaining hardening is tracked under #3400.
 - [`canonical-session-resolution.md`](canonical-session-resolution.md) — #2361
   focused contract for resolving URL, query parameter, localStorage, sidebar,
   and compression-lineage session IDs to one canonical visible chat target.
diff --git a/docs/rfcs/live-to-final-assistant-replies.md b/docs/rfcs/live-to-final-assistant-replies.md
index 68e8093dd..6564390e8 100644
--- a/docs/rfcs/live-to-final-assistant-replies.md
+++ b/docs/rfcs/live-to-final-assistant-replies.md
@@ -3,6 +3,7 @@
 - **Status:** Accepted (parent contract; implementation tracked in [#3400](https://github.com/nesquena/hermes-webui/issues/3400))
 - **Author:** @franksong2702
 - **Created:** 2026-06-03
+- **Updated:** 2026-07-16
 - **Tracking issue:** [#3400](https://github.com/nesquena/hermes-webui/issues/3400)
 
 ## Background: Long-Running Sessions Are The Anchor
@@ -204,6 +205,43 @@ Requirements:
 - Very long final answers remain complete and readable. They should not be
   hidden inside the activity summary or replaced by a progress/status artifact.
 
+### Activity display and disclosure addenda
+
+The accepted lifecycle now has three presentation strategies over the same
+assistant-turn activity data:
+
+- **Compact Worklog** remains the default. Its top-level Worklog is expanded
+  while live so progress remains visible, and the user may collapse or reopen it.
+  Nested tool/reasoning detail remains progressively disclosed.
+- **Transparent Stream** is opt-in and renders the same ordered activity as
+  chronological rows. It does not create a second live or settled owner.
+- **Final answer only** is opt-in (`hide_all_activity` in persisted settings).
+  It suppresses activity rows without deleting the persisted Anchor scene or
+  changing the final-answer owner.
+
+For normal completed turns, the settled Compact Worklog remains collapsed by
+default. When a terminal error-family turn has actual Worklog content, the
+Worklog defaults open so readable partial work is not hidden behind the error
+outcome. The current disclosure error family is `error`, `no_response`,
+`degraded`, `connection_lost`, `tool_limit_reached`, and
+`compression_exhausted`; cancelled turns and the parent `interrupted` terminal
+outcome keep their separate semantics. An explicit user disclosure choice wins
+over these defaults and may be restored across a render rebuild.
+
+`degraded` and `connection_lost` are Anchor-level reconstruction/transport
+outcomes defined in
+[`stable-assistant-turn-anchors.md`](stable-assistant-turn-anchors.md), not
+additional canonical product states in the table below. In this parent
+contract, `connection_lost` is the transport-specific Anchor form of an
+interruption, while `degraded` is the explicit recovery-state counterpart to the
+restoring/degraded path. They use error-family disclosure only because they can
+leave readable partial Worklog content without a normal final answer.
+
+These are presentation and disclosure rules only. They do not change reply
+ownership, terminal classification, durable transcript truth, or the requirement
+that all three strategies converge across live, settle, reload, session switch,
+and reconnect.
+
 ### Recovery and replay
 
 Refresh, reconnect, session switching, and replay should preserve the same
@@ -473,7 +511,9 @@ for current open/merged/superseded status.
 | Track | Scope | Current vehicle |
 | --- | --- | --- |
 | Parent product RFC | Define the long-running live-to-final assistant reply lifecycle and review checklist. | This RFC; tracking issue [#3400](https://github.com/nesquena/hermes-webui/issues/3400). |
-| First reply lifecycle implementation | Live process prose, quiet tool activity, settled activity summary above final answer, replay/reattach consistency, live-only compression status, supporting stream ownership fixes. | [#3401](https://github.com/nesquena/hermes-webui/pull/3401). |
+| First reply lifecycle implementation | Live process prose, quiet tool activity, settled activity summary above final answer, replay/reattach consistency, live-only compression status, supporting stream ownership fixes. | [#3401](https://github.com/nesquena/hermes-webui/pull/3401), absorbed through [#3741](https://github.com/nesquena/hermes-webui/pull/3741). |
+| Activity display projections | Compact Worklog by default, opt-in Transparent Stream, and opt-in Final answer only over the same assistant-turn data. | [#3820](https://github.com/nesquena/hermes-webui/issues/3820), [`transparent-stream-activity-mode.md`](transparent-stream-activity-mode.md), tracking issue [#3400](https://github.com/nesquena/hermes-webui/issues/3400). |
+| Assistant-turn presentation ownership | Normalize live, settled, replayed, and recovered activity into one Anchor / `activity_scene_v1`, with legacy rendering limited to historical or non-anchor compatibility. | [#3926](https://github.com/nesquena/hermes-webui/issues/3926), [`stable-assistant-turn-anchors.md`](stable-assistant-turn-anchors.md); core implementation shipped through the #4411/#4564 and #5242/#5243 capstones. |
 | Terminal/no-final stabilization | Compression exhausted, tool-tail/no-final transcript shape, context-compaction marker suppression, terminal error routing. | [#3315](https://github.com/nesquena/hermes-webui/issues/3315), [#3316](https://github.com/nesquena/hermes-webui/pull/3316). |
 | Cancel ownership hardening | Frontend cancel should close its own SSE source and clear only its own busy state. | [#3344](https://github.com/nesquena/hermes-webui/issues/3344), [#3345](https://github.com/nesquena/hermes-webui/pull/3345). |
 | Early-cancel startup race | Backend cancel should still interrupt the worker when the SSE registry detached before startup fully settled. | [#3475](https://github.com/nesquena/hermes-webui/issues/3475), [#3476](https://github.com/nesquena/hermes-webui/pull/3476). |
diff --git a/docs/rfcs/stable-assistant-turn-anchors.md b/docs/rfcs/stable-assistant-turn-anchors.md
index 7fea9e301..9c522519b 100644
--- a/docs/rfcs/stable-assistant-turn-anchors.md
+++ b/docs/rfcs/stable-assistant-turn-anchors.md
@@ -1,12 +1,35 @@
 # Stable Assistant Turn Anchors for Live-to-Final Rendering
 
-- **Status:** Proposed
+- **Status:** Implemented
 - **Author:** @franksong2702
 - **Created:** 2026-06-10
+- **Updated:** 2026-07-16
 - **Tracking issue:** [#3926](https://github.com/nesquena/hermes-webui/issues/3926)
 - **Parent contract:** [Live-to-Final Assistant Replies](./live-to-final-assistant-replies.md) ([#3400](https://github.com/nesquena/hermes-webui/issues/3400))
 - **Related RFCs:** [Transparent Stream](./transparent-stream-activity-mode.md), [Hermes Run Adapter Contract](./hermes-run-adapter-contract.md), [WebUI Run State Consistency Contract](./webui-run-state-consistency-contract.md), [Turn Journal](./turn-journal.md), [Pending Intent Controls](./webui-pending-intent-controls.md)
 
+## Implementation Status
+
+The RFC's core presentation/reconciliation path is implemented. Current
+`master` includes the event normalizer and registry, settled final-answer
+projection, ordered `activity_scene_v1`, live Compact Worklog rendering,
+Transparent Stream rendering, run-journal hydration, session re-entry,
+transcript-backed scene persistence, and explicit fallback ownership for
+historical or non-anchor transcripts.
+
+`Implemented` does not mean every adjacent hardening item is complete. The
+remaining work is tracked under [#3400](https://github.com/nesquena/hermes-webui/issues/3400)
+and should land as separate slices:
+
+- replace presentation-layer text/prefix de-echo heuristics with provenance or
+  event identity without deleting legitimate repeated model output;
+- make newer journal/replay evidence explicitly outrank stale `INFLIGHT`
+  first-paint state;
+- finish stable `run_id` versus transport `stream_id` separation;
+- complete the Phase 6 Artifact/side-effect ownership path;
+- remove each legacy fallback only after its historical transcript shape can
+  hydrate an Anchor reliably.
+
 ## Problem
 
 The Live-to-Final redesign made the user-facing product model clearer:
@@ -763,6 +786,11 @@ Implementation PRs may combine adjacent low-risk phases when they preserve
 behavior and include coverage. Settlement, reconstruction, and display-mode
 changes should remain independently reviewable.
 
+Implementation reconciliation (2026-07-16): the core Phase 0-5 path has shipped.
+Phase 6 and the hardening items listed in **Implementation Status** remain
+follow-up work; the phase descriptions below are retained as the rollout
+contract that produced the current implementation.
+
 ### Phase 0: RFC and inventory
 
 - Land this RFC as design guidance.
@@ -902,6 +930,11 @@ Any implementation PR against this RFC should answer:
 
 ## Open Questions
 
+The first-slice and Transparent Stream sequencing questions below are retained
+as historical implementation rationale. Current open hardening questions are
+identity fallback depth, Artifact/side-effect ownership, and how far active-turn
+DOM rebuilds can be reduced without weakening recovery compatibility.
+
 ### First implementation slice size
 
 Should the first implementation PR stop at hidden anchor scaffolding, or should
diff --git a/docs/rfcs/transparent-stream-activity-mode.md b/docs/rfcs/transparent-stream-activity-mode.md
index c844b5781..9909c634b 100644
--- a/docs/rfcs/transparent-stream-activity-mode.md
+++ b/docs/rfcs/transparent-stream-activity-mode.md
@@ -1,12 +1,31 @@
 # Transparent Stream — A Chronological Activity Display Mode
 
-- **Status:** Accepted (direction confirmed by @nesquena; RFC merged via [#3862](https://github.com/nesquena/hermes-webui/pull/3862))
+- **Status:** Implemented (opt-in display mode; follow-up hardening tracked in [#3400](https://github.com/nesquena/hermes-webui/issues/3400))
 - **Author:** @franksong2702
 - **Created:** 2026-06-09
-- **Updated:** 2026-06-09
+- **Updated:** 2026-07-16
 - **Tracking issue:** [#3820](https://github.com/nesquena/hermes-webui/issues/3820)
 - **Parent contract:** [Live-to-Final Assistant Replies](./live-to-final-assistant-replies.md) ([#3400](https://github.com/nesquena/hermes-webui/issues/3400) / #3401 / #3741)
 
+## Current projection family
+
+The shipped `chat_activity_display_mode` setting now has three explicit values:
+
+- `compact_worklog` — default, results-first presentation;
+- `transparent_stream` — opt-in chronological activity rows;
+- `hide_all_activity` — opt-in **Final answer only** presentation.
+
+All three are render strategies over the same Assistant Turn Anchor and
+`activity_scene_v1`; they do not create separate activity ownership or change
+the final-answer boundary. Final answer only suppresses activity presentation
+while preserving the persisted scene so another mode, settle, or reload can
+reconstruct the same turn.
+
+The original proposal and rollout notes below are retained as design history.
+Statements describing a missing selector, missing settled branch, or unwired
+live/replay renderer describe the tree when this RFC was written, not current
+`master`.
+
 ## Problem
 
 After the live-to-final redesign (#3401/#3741), the execution trace of a turn
@@ -104,21 +123,22 @@ Plus two boundaries:
 - **Not full transcript virtualization.** Performance hardening for very long
   transparent transcripts (#3714) is acknowledged but scoped to a later slice.
 
-## Proposal
+## Implemented proposal
 
 ### 1. A new, dedicated preference
 
-A new preference, independent of `simplified_tool_calling`:
+The shipped preference is independent of `simplified_tool_calling`:
 
 ```python
 # api/config.py preferences
-"chat_activity_display_mode": "compact_worklog",  # | "transparent_stream"
+"chat_activity_display_mode": "compact_worklog",  # | "transparent_stream" | "hide_all_activity"
 ```
 
 - Default `compact_worklog` — existing users see no change.
 - Surfaced in Settings as an explicit **segmented choice** (not a checkbox):
   - **Compact Worklog** — default; results-first, supporting activity quiet.
   - **Transparent Stream** — advanced; every step shown chronologically.
+  - **Final answer only** — activity hidden; final answer remains visible.
 - The legacy `Compact tool activity` checkbox is marked deprecated. It is not
   the seam for this feature.
 
@@ -128,6 +148,7 @@ predicate used everywhere:
 ```js
 function chatActivityMode(){ return window._chatActivityDisplayMode || 'compact_worklog'; }
 function isTransparentStream(){ return chatActivityMode() === 'transparent_stream'; }
+function isFinalAnswerOnlyMode(){ return chatActivityMode() === 'hide_all_activity'; }
 ```
 
 ### 2. Decouple "event sequence" from "grouping strategy"
diff --git a/docs/rfcs/webui-run-state-consistency-contract.md b/docs/rfcs/webui-run-state-consistency-contract.md
index 6a3c839fb..a14bc5205 100644
--- a/docs/rfcs/webui-run-state-consistency-contract.md
+++ b/docs/rfcs/webui-run-state-consistency-contract.md
@@ -3,8 +3,9 @@
 - **Status:** Proposed
 - **Author:** @franksong2702
 - **Created:** 2026-05-16
+- **Updated:** 2026-07-16
 - **Tracking issue:** [#2361](https://github.com/nesquena/hermes-webui/issues/2361)
-- **Related architecture:** [#1925](https://github.com/nesquena/hermes-webui/issues/1925), [`hermes-run-adapter-contract.md`](hermes-run-adapter-contract.md)
+- **Related architecture:** [#1925](https://github.com/nesquena/hermes-webui/issues/1925), [`hermes-run-adapter-contract.md`](hermes-run-adapter-contract.md), [`stable-assistant-turn-anchors.md`](stable-assistant-turn-anchors.md)
 
 ## Problem
 
@@ -46,6 +47,21 @@ while WebUI still has multiple overlapping state stores.
 - Do not reopen already-fixed narrow bugs.
 - Do not make this a catch-all for unrelated UI polish.
 
+## Current implementation relationship
+
+Stable Assistant Turn Anchors now implement the presentation/reconciliation
+portion of this contract for one assistant turn. The run journal and settled
+transcript provide durable observations; the Anchor registry and
+`activity_scene_v1` reconcile those observations into Compact Worklog,
+Transparent Stream, or Final answer only; `S.messages`, `INFLIGHT`, renderer
+caches, and DOM remain projections or recovery caches rather than independent
+semantic owners.
+
+This RFC remains `Proposed` because its broader cross-layer contract also covers
+model-context reconstruction, compression handoff, session metadata, and future
+runtime-adapter migration. Shipped Anchor coverage strengthens invariants 2, 3,
+and 5; it does not mark every run-state boundary implemented.
+
 ## State Layers
 
 | Layer | Purpose | Source-of-truth expectation | Must not do |
diff --git a/docs/troubleshooting.md b/docs/troubleshooting.md
index 71d63d73a..5d0e7ea6a 100644
--- a/docs/troubleshooting.md
+++ b/docs/troubleshooting.md
@@ -177,6 +177,28 @@ turn in the exhausted session instead of being blocked with recovery guidance.
 
 ---
 
+## "Hermes Agent was updated while Hermes WebUI was running"
+
+**Symptom.** An action that uses the in-process Agent runtime stops with a message telling you to restart Hermes WebUI. This can happen after `hermes update`, a Git checkout/pull in the Agent source tree, or another tool updates Hermes Agent without restarting the already-running WebUI backend.
+
+**Why.** WebUI currently imports `run_agent.AIAgent` into its long-lived Python process. Python keeps imported modules in memory. Continuing after a known Agent Git revision changes could combine cached modules from the old revision with source read from the new revision, producing misleading `ImportError`s or inconsistent runtime state. For local Agent-backed chat, WebUI therefore returns a retryable `409 agent_runtime_stale` before claiming or mutating session state instead of attempting a partial in-process reload. Gateway-backed chat runs in the gateway process and is not blocked by this WebUI-local check. Non-Git Agent installs preserve their existing behavior because there is no revision identity to compare.
+
+**Diagnostic.** Compare the running WebUI process start time with the Agent checkout revision and recent update history. If the Agent was updated after WebUI started, restart WebUI before investigating individual missing-symbol errors.
+
+**Fix.** Restart using the same launch method that started WebUI:
+
+```bash
+./ctl.sh restart
+# Or, for a user systemd service:
+systemctl --user restart hermes-webui.service
+```
+
+If you launched `python3 bootstrap.py` in the foreground, stop it with Ctrl-C and start it again. Restarting the whole computer or WSL is not required when restarting the WebUI backend succeeds.
+
+**When to file a bug.** File a WebUI bug if the restart-required message appears even though the Agent revision did not change, or if a clean WebUI restart still produces the same import error. Include the WebUI launch method, WebUI revision, Agent revision, and the sanitized error text.
+
+---
+
 ## Other troubleshooting
 
 This document grows over time. If a recurring failure mode isn't covered here yet, add it via PR. The format for each entry: **Symptom → Why → Diagnostic commands → Fix → When to file a bug**.
diff --git a/static/assistant_turn_anchors.js b/static/assistant_turn_anchors.js
index 7c11ca1f5..17c69ba0f 100644
--- a/static/assistant_turn_anchors.js
+++ b/static/assistant_turn_anchors.js
@@ -1,9 +1,9 @@
-// Stable Assistant Turn Anchors scaffold (#3926).
+// Stable Assistant Turn Anchors implementation (#3926 / #3400).
 //
-// This file defines the current ownership inventory, event classifications, and
-// small owner helpers. It does not register anchors globally. The only renderer
-// wiring in this slice is settled assistant final-answer projection; live
-// streaming, replay hydration, tools, and DOM ownership remain unwired.
+// This file defines the ownership inventory, event normalization, registry, and
+// activity-scene projection consumed by current live, settled, replay-hydration,
+// and session-reentry paths. Runtime execution and transport remain outside the
+// Anchor's presentation/reconciliation ownership boundary.
 (function(){
   const ROOT=(typeof window!=='undefined')?window:globalThis;
 
diff --git a/tests/test_agent_runtime_revision_guard.py b/tests/test_agent_runtime_revision_guard.py
new file mode 100644
index 000000000..9712f711f
--- /dev/null
+++ b/tests/test_agent_runtime_revision_guard.py
@@ -0,0 +1,687 @@
+"""Regression coverage for Hermes Agent source changes during a WebUI process lifetime."""
+
+from __future__ import annotations
+
+import os
+from pathlib import Path
+import subprocess
+import sys
+import types
+
+import pytest
+
+
+REPO = Path(__file__).resolve().parents[1]
+
+
+def _git(repo: Path, *args: str) -> str:
+    result = subprocess.run(
+        ["git", "-c", "user.name=Test", "-c", "user.email=test@example.invalid", *args],
+        cwd=repo,
+        check=True,
+        capture_output=True,
+        text=True,
+    )
+    return result.stdout.strip()
+
+
+def test_loaded_agent_runtime_fails_closed_after_source_revision_changes(tmp_path: Path):
+    agent_dir = tmp_path / "hermes-agent"
+    agent_dir.mkdir()
+    (agent_dir / "run_agent.py").write_text(
+        "class AIAgent:\n    revision = 'before'\n",
+        encoding="utf-8",
+    )
+    _git(agent_dir, "init", "-q")
+    _git(agent_dir, "add", "run_agent.py")
+    _git(agent_dir, "commit", "-qm", "before")
+
+    probe = tmp_path / "probe.py"
+    probe.write_text(
+        """
+from pathlib import Path
+import subprocess
+
+import api.streaming as streaming
+from api import agent_runtime
+
+agent_dir = Path(__file__).parent / "hermes-agent"
+assert agent_runtime._AGENT_DIR == agent_dir.resolve()
+assert streaming._get_ai_agent().revision == "before"
+
+(agent_dir / "run_agent.py").write_text(
+    "class AIAgent:\\n    revision = 'after'\\n",
+    encoding="utf-8",
+)
+subprocess.run(["git", "add", "run_agent.py"], cwd=agent_dir, check=True)
+subprocess.run(
+    [
+        "git", "-c", "user.name=Test", "-c", "user.email=test@example.invalid",
+        "commit", "-qm", "after",
+    ],
+    cwd=agent_dir,
+    check=True,
+)
+
+try:
+    streaming._get_ai_agent()
+except RuntimeError as exc:
+    message = str(exc)
+    assert "Hermes Agent was updated" in message
+    assert "Restart Hermes WebUI" in message
+else:
+    raise AssertionError("stale in-process AIAgent was reused after its source revision changed")
+
+try:
+    agent_runtime.require_ai_agent_class()
+except agent_runtime.AgentRuntimeChangedError as exc:
+    assert "Restart Hermes WebUI" in str(exc)
+else:
+    raise AssertionError("unguarded AIAgent import was allowed after its source revision changed")
+""".strip()
+        + "\n",
+        encoding="utf-8",
+    )
+
+    env = os.environ.copy()
+    env.update(
+        {
+            "HERMES_WEBUI_AGENT_DIR": str(agent_dir),
+            "HERMES_HOME": str(tmp_path / "hermes-home"),
+            "HERMES_WEBUI_STATE_DIR": str(tmp_path / "webui-state"),
+            "PYTHONPATH": os.pathsep.join((str(REPO), str(agent_dir))),
+        }
+    )
+    result = subprocess.run(
+        [sys.executable, str(probe)],
+        cwd=REPO,
+        env=env,
+        capture_output=True,
+        text=True,
+        timeout=30,
+    )
+
+    assert result.returncode == 0, result.stdout + result.stderr
+
+
+def test_initial_non_git_source_preserves_supported_runtime(monkeypatch):
+    """Non-Git installs cannot be compared, so they preserve existing behavior."""
+    from api import agent_runtime
+
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", None)
+    monkeypatch.setattr(
+        agent_runtime,
+        "_read_agent_revision",
+        lambda _path, **_kwargs: None,
+    )
+
+    agent_runtime.ensure_agent_runtime_current()
+
+
+def test_untracked_loaded_module_inside_outer_git_repo_is_non_git(
+    monkeypatch, tmp_path: Path
+):
+    """An enclosing unrelated Git repo must not identify an installed module."""
+    from api import agent_runtime
+
+    outer_repo = tmp_path / "outer-repo"
+    module_dir = outer_repo / "installed" / "hermes-agent"
+    module_dir.mkdir(parents=True)
+    module_file = module_dir / "run_agent.py"
+    module_file.write_text("class AIAgent: pass\n", encoding="utf-8")
+    (outer_repo / "tracked.txt").write_text("unrelated\n", encoding="utf-8")
+    _git(outer_repo, "init", "-q")
+    _git(outer_repo, "add", "tracked.txt")
+    _git(outer_repo, "commit", "-qm", "unrelated")
+
+    loaded_module = types.ModuleType("run_agent")
+    loaded_module.__file__ = str(module_file)
+    monkeypatch.setitem(sys.modules, "run_agent", loaded_module)
+    monkeypatch.setattr(agent_runtime, "_AGENT_SOURCE_DIR", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_MODULE_PATH", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", None)
+
+    agent_runtime._capture_loaded_agent_revision()
+
+    assert agent_runtime._AGENT_SOURCE_DIR == module_dir.resolve()
+    assert agent_runtime._AGENT_MODULE_PATH == module_file.resolve()
+    assert agent_runtime._AGENT_REVISION is None
+
+    (outer_repo / "tracked.txt").write_text("unrelated change\n", encoding="utf-8")
+    _git(outer_repo, "add", "tracked.txt")
+    _git(outer_repo, "commit", "-qm", "unrelated change")
+
+    agent_runtime.ensure_agent_runtime_current()
+
+
+def test_untracked_module_pathspec_metacharacters_are_literal(monkeypatch, tmp_path: Path):
+    """Git pathspec syntax must not turn an untracked module into a tracked match."""
+    from api import agent_runtime
+
+    outer_repo = tmp_path / "outer-repo"
+    tracked_dir = outer_repo / "installed" / "agent"
+    untracked_dir = outer_repo / "installed" / "[a]gent"
+    tracked_dir.mkdir(parents=True)
+    untracked_dir.mkdir(parents=True)
+    (tracked_dir / "run_agent.py").write_text("class Other: pass\n", encoding="utf-8")
+    module_file = untracked_dir / "run_agent.py"
+    module_file.write_text("class AIAgent: pass\n", encoding="utf-8")
+    _git(outer_repo, "init", "-q")
+    _git(outer_repo, "add", "installed/agent/run_agent.py")
+    _git(outer_repo, "commit", "-qm", "tracked lookalike")
+
+    loaded_module = types.ModuleType("run_agent")
+    loaded_module.__file__ = str(module_file)
+    monkeypatch.setitem(sys.modules, "run_agent", loaded_module)
+    monkeypatch.setattr(agent_runtime, "_AGENT_SOURCE_DIR", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_MODULE_PATH", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", None)
+
+    agent_runtime._capture_loaded_agent_revision()
+
+    assert agent_runtime._AGENT_SOURCE_DIR == untracked_dir.resolve()
+    assert agent_runtime._AGENT_MODULE_PATH == module_file.resolve()
+    assert agent_runtime._AGENT_REVISION is None
+
+
+def test_revision_identity_comes_from_loaded_agent_module(monkeypatch, tmp_path: Path):
+    """The configured discovery path must not override the loaded module path."""
+    from api import agent_runtime
+
+    configured_dir = tmp_path / "configured-agent"
+    loaded_dir = tmp_path / "loaded-agent"
+    for agent_dir, revision in ((configured_dir, "configured"), (loaded_dir, "loaded")):
+        agent_dir.mkdir()
+        (agent_dir / "run_agent.py").write_text(
+            f"class AIAgent:\n    revision = '{revision}'\n",
+            encoding="utf-8",
+        )
+        _git(agent_dir, "init", "-q")
+        _git(agent_dir, "add", "run_agent.py")
+        _git(agent_dir, "commit", "-qm", revision)
+
+    loaded_module = types.ModuleType("run_agent")
+    loaded_module.__file__ = str(loaded_dir / "run_agent.py")
+    monkeypatch.setitem(sys.modules, "run_agent", loaded_module)
+    monkeypatch.setattr(agent_runtime, "_AGENT_DIR", configured_dir)
+    monkeypatch.setattr(agent_runtime, "_AGENT_SOURCE_DIR", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_MODULE_PATH", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", None)
+
+    agent_runtime._capture_loaded_agent_revision()
+
+    assert agent_runtime._AGENT_SOURCE_DIR == loaded_dir.resolve()
+    assert agent_runtime._AGENT_MODULE_PATH == (loaded_dir / "run_agent.py").resolve()
+    assert agent_runtime._AGENT_REVISION == _git(loaded_dir, "rev-parse", "HEAD")
+
+
+def test_known_revision_becoming_unreadable_fails_closed(monkeypatch):
+    """Losing a previously-known revision is indistinguishable from source drift."""
+    from api import agent_runtime
+
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", "known-revision")
+    monkeypatch.setattr(
+        agent_runtime,
+        "_read_agent_revision",
+        lambda _path, **_kwargs: None,
+    )
+
+    with pytest.raises(agent_runtime.AgentRuntimeChangedError):
+        agent_runtime.ensure_agent_runtime_current()
+
+
+def test_import_recapture_cannot_downgrade_known_revision(monkeypatch, tmp_path: Path):
+    """A second unreadable revision read must not erase a known identity."""
+    from api import agent_runtime
+
+    source_dir = tmp_path / "loaded-agent"
+    source_dir.mkdir()
+    loaded_module = types.ModuleType("run_agent")
+    loaded_module.__file__ = str(source_dir / "run_agent.py")
+    loaded_module.__dict__["AIAgent"] = type("AIAgent", (), {})
+    monkeypatch.setitem(sys.modules, "run_agent", loaded_module)
+    monkeypatch.setattr(agent_runtime, "_AGENT_SOURCE_DIR", source_dir.resolve())
+    monkeypatch.setattr(agent_runtime, "_AGENT_MODULE_PATH", source_dir / "run_agent.py")
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", "known-revision")
+    revisions = iter(("known-revision", None))
+    monkeypatch.setattr(
+        agent_runtime,
+        "_read_agent_revision",
+        lambda _path, **_kwargs: next(revisions),
+    )
+
+    with pytest.raises(agent_runtime.AgentRuntimeChangedError):
+        agent_runtime.require_ai_agent_class()
+
+    assert agent_runtime._AGENT_REVISION == "known-revision"
+
+
+def test_in_memory_agent_swap_does_not_mimic_source_revision_change(
+    monkeypatch, tmp_path: Path
+):
+    """Only the bound checkout revision, not ``sys.modules`` swaps, defines staleness."""
+    from api import agent_runtime
+
+    agent_dir = tmp_path / "loaded-agent"
+    agent_dir.mkdir()
+    module_file = agent_dir / "run_agent.py"
+    module_file.write_text("class AIAgent: pass\n", encoding="utf-8")
+    _git(agent_dir, "init", "-q")
+    _git(agent_dir, "add", "run_agent.py")
+    _git(agent_dir, "commit", "-qm", "loaded agent")
+
+    loaded_module = types.ModuleType("run_agent")
+    loaded_module.__file__ = str(module_file)
+    loaded_module.__dict__["AIAgent"] = type("LoadedAgent", (), {})
+    monkeypatch.setitem(sys.modules, "run_agent", loaded_module)
+    monkeypatch.setattr(agent_runtime, "_AGENT_SOURCE_DIR", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_MODULE_PATH", None)
+    monkeypatch.setattr(agent_runtime, "_AGENT_REVISION", None)
+    agent_runtime._capture_loaded_agent_revision()
+
+    replacement_class = type("ReplacementAgent", (), {})
+    replacement_module = types.ModuleType("run_agent")
+    replacement_module.__dict__["AIAgent"] = replacement_class
+    monkeypatch.setitem(sys.modules, "run_agent", replacement_module)
+
+    assert agent_runtime.require_ai_agent_class() is replacement_class
+    assert agent_runtime._AGENT_SOURCE_DIR == agent_dir.resolve()
+    assert agent_runtime._AGENT_MODULE_PATH == module_file.resolve()
+    assert agent_runtime._AGENT_REVISION == _git(agent_dir, "rev-parse", "HEAD")
+
+
+def test_runner_local_bypasses_webui_agent_barrier(monkeypatch):
+    """Runner-local execution is owned by the runner, not this process."""
+    from api import routes
+
+    monkeypatch.setattr(routes, "webui_gateway_chat_enabled", lambda _cfg: False)
+    monkeypatch.setattr(routes, "get_config", lambda: {})
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            AssertionError("runner-local must not inspect the WebUI Agent checkout")
+        ),
+    )
+    monkeypatch.setattr(
+        "api.runtime_adapter.runtime_adapter_runner_enabled",
+        lambda: True,
+    )
+
+    assert routes._agent_runtime_barrier_response(runner_local_owned=True) is None
+
+
+def test_runner_flag_does_not_bypass_webui_owned_hidden_turns(monkeypatch):
+    """Runner/gateway modes do not transfer ownership of legacy hidden turns."""
+    from api import agent_runtime, routes
+
+    monkeypatch.setattr(routes, "webui_gateway_chat_enabled", lambda _cfg: True)
+    monkeypatch.setattr(routes, "get_config", lambda: {})
+    monkeypatch.setattr(
+        "api.runtime_adapter.runtime_adapter_runner_enabled",
+        lambda: True,
+    )
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            agent_runtime.AgentRuntimeChangedError("restart required")
+        ),
+    )
+
+    response = routes._agent_runtime_barrier_response(runner_local_owned=False)
+
+    assert response == {
+        "error": "restart required",
+        "type": "agent_runtime_stale",
+        "retryable": True,
+    }
+
+
+def test_chat_start_rejects_stale_runtime_before_session_materialization(monkeypatch):
+    """A stale local runtime must not claim, create, or mutate session state."""
+    from api import agent_runtime, routes
+
+    monkeypatch.setattr(routes, "webui_gateway_chat_enabled", lambda _cfg: False)
+    monkeypatch.setattr(routes, "get_config", lambda: {})
+
+    def stale():
+        raise agent_runtime.AgentRuntimeChangedError("restart required")
+
+    monkeypatch.setattr(routes, "ensure_agent_runtime_current", stale)
+
+    def must_not_materialize(*_args, **_kwargs):
+        raise AssertionError("session materialized before stale-runtime barrier")
+
+    monkeypatch.setattr(routes, "_get_or_materialize_session", must_not_materialize)
+    monkeypatch.setattr(
+        routes,
+        "j",
+        lambda _handler, payload, status=200: {"status": status, "payload": payload},
+    )
+
+    response = routes._handle_chat_start(object(), {"session_id": "session-1"})
+
+    assert response == {
+        "status": 409,
+        "payload": {
+            "error": "restart required",
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        },
+    }
+
+
+def test_runner_owned_start_run_does_not_enter_local_stream_barrier(monkeypatch):
+    """The runner adapter must not invoke the WebUI in-process delegate."""
+    from api import routes
+
+    calls = []
+
+    class RunnerClient:
+        def start_run(self, request):
+            calls.append(request)
+            return {
+                "run_id": "runner-run-1",
+                "stream_id": "runner-stream-1",
+                "session_id": request.session_id,
+                "status": "started",
+            }
+
+    session = types.SimpleNamespace(session_id="session-1", profile=None)
+    monkeypatch.setenv("HERMES_WEBUI_RUNTIME_ADAPTER", "runner-local")
+    monkeypatch.setattr("api.runtime_adapter.runtime_adapter_enabled", lambda: False)
+    monkeypatch.setattr("api.runtime_adapter.runtime_adapter_runner_enabled", lambda: True)
+    monkeypatch.setattr(routes, "_runtime_runner_client_factory", lambda: RunnerClient())
+    monkeypatch.setattr(
+        routes,
+        "_start_chat_stream_for_session",
+        lambda **_kwargs: (_ for _ in ()).throw(
+            AssertionError("runner-owned start entered the WebUI local stream path")
+        ),
+    )
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            AssertionError("runner-owned start inspected the WebUI Agent revision")
+        ),
+    )
+
+    response = routes._start_run(
+        session,
+        msg="hello",
+        attachments=[],
+        workspace="/tmp/workspace",
+        model="test-model",
+        model_provider="test-provider",
+        normalized_model=False,
+        source="webui",
+        route="/api/chat/start",
+    )
+
+    assert response.get("stream_id") == "runner-stream-1", response
+    assert len(calls) == 1
+
+
+@pytest.mark.parametrize("gateway_owned", [False, True])
+def test_stream_admission_uses_one_gateway_ownership_snapshot(monkeypatch, gateway_owned):
+    """The barrier and worker must share one immutable backend decision."""
+    from api import routes
+    from api import turn_journal
+    from api.config import unregister_stream_owner
+
+    gateway_reads = []
+    revision_checks = []
+    worker_targets = []
+    session = types.SimpleNamespace(
+        session_id="gateway-snapshot",
+        profile=None,
+        title="Gateway snapshot",
+        active_stream_id=None,
+        pending_started_at=None,
+    )
+
+    def read_gateway(_cfg):
+        gateway_reads.append(True)
+        if len(gateway_reads) > 1:
+            raise AssertionError("gateway ownership was re-read after admission")
+        return gateway_owned
+
+    def prepare(current, **kwargs):
+        current.active_stream_id = kwargs["stream_id"]
+        current.pending_started_at = 123.0
+
+    class FakeThread:
+        def __init__(self, *, target, args, kwargs, daemon):
+            worker_targets.append(target)
+
+        def start(self):
+            return None
+
+    monkeypatch.setattr(routes, "webui_gateway_chat_enabled", read_gateway)
+    monkeypatch.setattr(routes, "get_config", lambda: {})
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: revision_checks.append(True),
+    )
+    monkeypatch.setattr(routes, "_active_run_stream_for_session", lambda _sid: None)
+    monkeypatch.setattr(routes, "_is_hidden_empty_session", lambda _session: False)
+    monkeypatch.setattr(routes, "_prepare_chat_start_session_for_stream", prepare)
+    monkeypatch.setattr(routes, "set_last_workspace", lambda _workspace: None)
+    monkeypatch.setattr(routes.threading, "Thread", FakeThread)
+    monkeypatch.setattr(turn_journal, "append_turn_journal_event", lambda *_args, **_kwargs: {})
+
+    response = routes._start_chat_stream_for_session(
+        session,
+        msg="goal",
+        attachments=[],
+        workspace="/tmp/workspace",
+        model="test-model",
+        goal_related=True,
+    )
+
+    try:
+        assert response["session_id"] == session.session_id
+        assert len(gateway_reads) == 1
+        assert revision_checks == ([] if gateway_owned else [True])
+        expected_worker = (
+            routes._run_gateway_chat_streaming
+            if gateway_owned
+            else routes._run_agent_streaming
+        )
+        assert worker_targets == [expected_worker]
+    finally:
+        stream_id = str(response.get("stream_id") or "")
+        with routes.STREAMS_LOCK:
+            routes.STREAMS.pop(stream_id, None)
+        unregister_stream_owner(stream_id)
+        routes.STREAM_GOAL_RELATED.pop(stream_id, None)
+
+
+@pytest.mark.parametrize(
+    ("handler_name", "body"),
+    [
+        ("_handle_git_commit_message", {"session_id": "git-message"}),
+        (
+            "_handle_git_commit_message_selected",
+            {"session_id": "git-message", "paths": ["selected.py"]},
+        ),
+    ],
+)
+def test_git_commit_message_stale_runtime_returns_typed_409(
+    monkeypatch, tmp_path, handler_name, body
+):
+    """Commit-message generation must preserve the stale-runtime contract."""
+    from api import routes
+    from api import workspace_git
+
+    session = types.SimpleNamespace(workspace=str(tmp_path))
+    monkeypatch.setattr(routes, "require", lambda _body, *keys: None)
+    monkeypatch.setattr(routes, "get_session", lambda _sid: session)
+    monkeypatch.setattr(routes, "_git_paths_from_body", lambda _body: ["selected.py"])
+    monkeypatch.setattr(
+        workspace_git,
+        "staged_commit_message_prompt",
+        lambda _workspace: {"system_prompt": "system", "user_prompt": "user"},
+    )
+    monkeypatch.setattr(
+        workspace_git,
+        "selected_commit_message_prompt",
+        lambda _workspace, _paths: {
+            "system_prompt": "system",
+            "user_prompt": "user",
+        },
+    )
+    monkeypatch.setattr(
+        routes,
+        "_llm_git_commit_message",
+        lambda *_args, **_kwargs: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+    monkeypatch.setattr(
+        routes,
+        "j",
+        lambda _handler, payload, status=200, **_kwargs: {
+            "status": status,
+            "payload": payload,
+        },
+    )
+    monkeypatch.setattr(
+        routes,
+        "bad",
+        lambda _handler, message, status=400: {
+            "status": status,
+            "payload": {"error": message},
+        },
+    )
+
+    response = getattr(routes, handler_name)(object(), body)
+
+    assert response == {
+        "status": 409,
+        "payload": {
+            "error": "restart required",
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        },
+    }
+
+
+def test_gateway_owned_start_run_bypasses_local_runtime_barrier(monkeypatch):
+    """Gateway chat must reach its worker without inspecting the local Agent."""
+    from api import routes
+
+    session = types.SimpleNamespace(session_id="session-1", profile=None)
+    captured = {}
+    monkeypatch.setattr("api.runtime_adapter.runtime_adapter_enabled", lambda: False)
+    monkeypatch.setattr("api.runtime_adapter.runtime_adapter_runner_enabled", lambda: False)
+    monkeypatch.setattr(routes, "webui_gateway_chat_enabled", lambda _cfg: True)
+    monkeypatch.setattr(routes, "get_config", lambda: {})
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            AssertionError("gateway-owned start inspected the WebUI Agent revision")
+        ),
+    )
+
+    def start_gateway(_session, **kwargs):
+        captured.update(kwargs)
+        return {"stream_id": "gateway-stream-1", "session_id": "session-1"}
+
+    monkeypatch.setattr(routes, "_start_chat_stream_for_session", start_gateway)
+
+    response = routes._start_run(
+        session,
+        msg="hello",
+        attachments=[],
+        workspace="/tmp/workspace",
+        model="test-model",
+        model_provider="test-provider",
+        normalized_model=False,
+        source="webui",
+        route="/api/chat/start",
+    )
+
+    assert response["stream_id"] == "gateway-stream-1"
+    assert captured["external_runtime_owned"] is True
+
+
+@pytest.mark.parametrize(
+    ("route", "body"),
+    [
+        ("_handle_btw", {"session_id": "session-1", "question": "question"}),
+        ("_handle_background", {"session_id": "session-1", "prompt": "prompt"}),
+        ("_handle_chat_sync", {"session_id": "session-1", "message": "message"}),
+    ],
+)
+def test_hidden_turn_routes_reject_stale_runtime_before_session_creation(
+    monkeypatch, route, body
+):
+    """Hidden-turn endpoints must reject before creation even in gateway mode."""
+    from api import routes
+
+    monkeypatch.setattr(routes, "webui_gateway_chat_enabled", lambda _cfg: True)
+    monkeypatch.setattr(routes, "get_config", lambda: {})
+    monkeypatch.setattr(
+        "api.runtime_adapter.runtime_adapter_runner_enabled",
+        lambda: True,
+    )
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+    monkeypatch.setattr(
+        routes,
+        "j",
+        lambda _handler, payload, status=200: {"status": status, "payload": payload},
+    )
+    monkeypatch.setattr(
+        routes,
+        "get_session",
+        lambda *_args, **_kwargs: (_ for _ in ()).throw(
+            AssertionError("session loaded before stale-runtime barrier")
+        ),
+    )
+
+    response = getattr(routes, route)(object(), body)
+
+    assert response["status"] == 409
+    assert response["payload"]["type"] == "agent_runtime_stale"
+
+
+def test_server_side_turn_rejects_stale_runtime_before_session_acceptance(monkeypatch):
+    """The direct process-wakeup entrypoint must fail before loading/mutating state."""
+    from api import routes
+
+    monkeypatch.setattr(
+        routes,
+        "_agent_runtime_barrier_response",
+        lambda **_kwargs: {
+            "error": "restart required",
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        },
+    )
+    monkeypatch.setattr(
+        routes,
+        "get_session",
+        lambda *_args, **_kwargs: (_ for _ in ()).throw(
+            AssertionError("session loaded before stale-runtime barrier")
+        ),
+    )
+
+    response = routes.start_session_turn("session-1", "wake up")
+
+    assert response == {
+        "error": "restart required",
+        "type": "agent_runtime_stale",
+        "retryable": True,
+        "_status": 409,
+    }
diff --git a/tests/test_agent_source_dependency_audit.py b/tests/test_agent_source_dependency_audit.py
index 9f56f5fb4..052673068 100644
--- a/tests/test_agent_source_dependency_audit.py
+++ b/tests/test_agent_source_dependency_audit.py
@@ -120,7 +120,7 @@ def test_audit_reports_runtime_agent_execution_imports():
     classes = _class_by_id(_run_audit())
     anchors = _anchors(classes["runtime_agent_execution"])
 
-    assert ("api/streaming.py", "run_agent") in anchors
+    assert ("api/agent_runtime.py", "run_agent") in anchors
     assert ("api/routes.py", "tools.skills_tool") in anchors
     assert ("api/streaming.py", "tools.approval") in anchors
     assert ("api/routes.py", "cron.jobs") in anchors
diff --git a/tests/test_cli_sessions_cache_cap.py b/tests/test_cli_sessions_cache_cap.py
new file mode 100644
index 000000000..7d2af868e
--- /dev/null
+++ b/tests/test_cli_sessions_cache_cap.py
@@ -0,0 +1,89 @@
+"""Tests: ``_CLI_SESSIONS_CACHE`` is LRU-bounded (drop-oldest).
+
+Regression: the CLI/cron session projection cache was a plain ``dict`` with TTL
+storage but NO size cap and only lazy, same-key eviction. Each value is a
+``copy.deepcopy()`` of the full CLI/cron session list (the expensive projection
+behind #4842/#4672). The cache key folds in a state.db content fingerprint that
+advances on every streamed message, so the next poll builds a NEW key; the
+previous key's heavy deepcopy was never looked up again, so its lazy-expiry path
+never ran. A long-lived process under churn could accumulate orphaned heavy
+deepcopies until the next structural ``clear_cli_sessions_cache()``.
+
+The cache is now an ``OrderedDict`` capped at ``_CLI_SESSIONS_CACHE_MAX_ENTRIES``
+with drop-oldest on write (mirroring ``_CLAUDE_CODE_PARSE_CACHE``) and
+``move_to_end`` on fresh hits. TTL remains the primary freshness control; the
+cap is the backstop the plain dict lacked.
+"""
+from __future__ import annotations
+
+import api.models as models
+from api.models import (
+    _CLI_SESSIONS_CACHE_MAX_ENTRIES,
+    _cache_cli_sessions_if_current,
+    _cli_sessions_cache_invalidation_stamp,
+    _copy_fresh_cli_sessions_cache_entry,
+)
+
+
+def _reset_cache():
+    with models._CLI_SESSIONS_CACHE_LOCK:
+        models._CLI_SESSIONS_CACHE.clear()
+
+
+def test_cache_is_bounded_drops_oldest_on_write():
+    """Inserting more than MAX_ENTRIES distinct keys keeps len == MAX and evicts
+    the OLDEST (least-recently-used) entry."""
+    _reset_cache()
+    stamp = _cli_sessions_cache_invalidation_stamp()
+    cap = _CLI_SESSIONS_CACHE_MAX_ENTRIES
+    assert cap >= 1
+
+    # Insert cap + 5 distinct keys, each a distinct payload so we can track them.
+    for i in range(cap + 5):
+        key = (f"profile-{i}",)
+        ok = _cache_cli_sessions_if_current(
+            key, ttl=60.0, invalidation_stamp=stamp, sessions=[{"id": i}]
+        )
+        assert ok
+
+    with models._CLI_SESSIONS_CACHE_LOCK:
+        assert len(models._CLI_SESSIONS_CACHE) == cap
+        keys = list(models._CLI_SESSIONS_CACHE.keys())
+    # The oldest 5 (profile-0..4) were evicted; the newest `cap` remain.
+    assert keys[0] == ("profile-5",)
+    assert keys[-1] == (f"profile-{cap + 5 - 1}",)
+    assert ("profile-0",) not in keys
+
+
+def test_fresh_hit_marks_entry_most_recently_used():
+    """A fresh cache hit moves the entry to the end (most-recently-used), so a
+    frequently-read entry is NOT evicted over colder ones."""
+    _reset_cache()
+    stamp = _cli_sessions_cache_invalidation_stamp()
+    cap = _CLI_SESSIONS_CACHE_MAX_ENTRIES
+
+    # Fill the cache exactly.
+    for i in range(cap):
+        _cache_cli_sessions_if_current(
+            (f"k{i}",), ttl=60.0, invalidation_stamp=stamp, sessions=[{"id": i}]
+        )
+    # Touch k0 (the oldest) so it becomes most-recently-used.
+    served = _copy_fresh_cli_sessions_cache_entry(("k0",))
+    assert served == [{"id": 0}]
+    # Now insert one more; the eviction victim should be k1, NOT k0.
+    _cache_cli_sessions_if_current(
+        ("k_new",), ttl=60.0, invalidation_stamp=stamp, sessions=[{"id": 999}]
+    )
+    with models._CLI_SESSIONS_CACHE_LOCK:
+        keys = list(models._CLI_SESSIONS_CACHE.keys())
+    assert ("k0",) in keys  # survived because it was just used
+    assert ("k1",) not in keys  # evicted as the new oldest
+    assert ("k_new",) in keys
+
+
+def test_cache_is_ordered_dict_not_plain_dict():
+    """The regression: the cache used to be a plain dict with no ordering. It
+    must now be an OrderedDict to support move_to_end / popitem(last=False)."""
+    import collections
+
+    assert isinstance(models._CLI_SESSIONS_CACHE, collections.OrderedDict)
diff --git a/tests/test_goal_command_webui.py b/tests/test_goal_command_webui.py
index 2389c08bc..b16f38926 100644
--- a/tests/test_goal_command_webui.py
+++ b/tests/test_goal_command_webui.py
@@ -161,7 +161,10 @@ def test_goal_continuation_decision_emits_status_and_normal_user_prompt(monkeypa
     assert decision["continuation_prompt"].startswith("[Continuing toward your standing goal]")
 
 
-def test_goal_endpoint_sets_goal_and_starts_kickoff_stream(monkeypatch, tmp_path):
+@pytest.mark.parametrize("gateway_owned", [False, True])
+def test_goal_endpoint_sets_goal_and_starts_kickoff_stream(
+    monkeypatch, tmp_path, gateway_owned
+):
     """POST /api/goal uses GoalManager state and launches the first goal turn."""
     from api import goals as webui_goals
     from api import routes
@@ -199,6 +202,12 @@ def test_goal_endpoint_sets_goal_and_starts_kickoff_stream(monkeypatch, tmp_path
     monkeypatch.setattr(webui_goals, "GoalManager", FakeGoalManager)
     monkeypatch.setattr(routes, "get_session", lambda sid: FakeSession())
     monkeypatch.setattr(routes, "resolve_trusted_workspace", lambda workspace: tmp_path)
+    monkeypatch.setattr(
+        routes,
+        "webui_gateway_chat_enabled",
+        lambda _cfg: gateway_owned,
+    )
+    monkeypatch.setattr(routes, "get_config", lambda: {})
     monkeypatch.setattr(
         routes,
         "_resolve_compatible_session_model_state",
@@ -229,6 +238,7 @@ def test_goal_endpoint_sets_goal_and_starts_kickoff_stream(monkeypatch, tmp_path
     assert result["payload"]["stream_id"] == "goal-stream"
     assert started and started[0]["msg"] == "ship the feature"
     assert started[0]["model_provider"] == "openai-codex"
+    assert started[0]["external_runtime_owned"] is gateway_owned
 
 
 def test_goal_endpoint_preserves_response_shape_under_runtime_adapter_flag(monkeypatch, tmp_path):
diff --git a/tests/test_issue1013_handoff_dock.py b/tests/test_issue1013_handoff_dock.py
index 39121ebc4..2a970bacc 100644
--- a/tests/test_issue1013_handoff_dock.py
+++ b/tests/test_issue1013_handoff_dock.py
@@ -248,6 +248,60 @@ def test_no_api_key_handoff_summary_persists_fallback_summary(monkeypatch):
     assert persisted[0]["rounds"] == models.CONVERSATION_ROUND_THRESHOLD
 
 
+def test_stale_runtime_handoff_summary_returns_typed_409_without_persisting(monkeypatch):
+    """A stale runtime must remain retryable instead of becoming fallback success."""
+    import api.routes as routes
+    import api.models as models
+
+    monkeypatch.setattr(routes, "require", lambda body, *keys: None)
+    monkeypatch.setattr(
+        routes,
+        "j",
+        lambda _handler, payload, status=200, extra_headers=None: {
+            "status": status,
+            "payload": payload,
+        },
+    )
+    monkeypatch.setattr(
+        models,
+        "count_conversation_rounds",
+        lambda sid, since=None: models.CONVERSATION_ROUND_THRESHOLD,
+    )
+    monkeypatch.setattr(
+        models,
+        "get_cli_session_messages",
+        lambda sid: [
+            {"role": "user", "content": "Need a handoff", "timestamp": 1.0},
+            {"role": "assistant", "content": "Context is ready", "timestamp": 2.0},
+        ],
+    )
+    monkeypatch.setattr(
+        routes,
+        "_persist_handoff_summary",
+        lambda *_args, **_kwargs: (_ for _ in ()).throw(
+            AssertionError("stale runtime persisted a fallback summary")
+        ),
+    )
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+
+    response = routes._handle_handoff_summary(object(), {"session_id": "stale-handoff"})
+
+    assert response == {
+        "status": 409,
+        "payload": {
+            "error": "restart required",
+            "type": "agent_runtime_stale",
+            "retryable": True,
+        },
+    }
+
+
 def test_exception_handoff_summary_persists_fallback_summary(monkeypatch):
     """Unhandled summary exception should still persist a fallback handoff marker."""
     import api.routes as routes
diff --git a/tests/test_regressions.py b/tests/test_regressions.py
index 827254297..8d38e4499 100644
--- a/tests/test_regressions.py
+++ b/tests/test_regressions.py
@@ -166,13 +166,13 @@ def test_streaming_py_imports_has_pending(cleanup_test_sessions):
 
 
 def test_aiagent_imported_in_streaming(cleanup_test_sessions):
-    """R2b: api/streaming.py must import AIAgent.
+    """R2b: api/streaming.py must resolve AIAgent through the runtime guard.
     When missing, the streaming thread crashed immediately after being spawned.
     """
     src = (REPO_ROOT / "api/streaming.py").read_text()
-    assert "AIAgent" in src, "AIAgent not referenced in api/streaming.py"
-    assert "from run_agent import AIAgent" in src or "import AIAgent" in src, \
-        "AIAgent must be imported in api/streaming.py"
+    assert "get_ai_agent_class" in src, "guarded AIAgent resolver not referenced in api/streaming.py"
+    assert "from api.agent_runtime import" in src and "get_ai_agent_class" in src, \
+        "AIAgent must be resolved through api.agent_runtime in api/streaming.py"
 
 
 # ── R5: SSE loop did not break on cancel event (Sprint 10 bug) ───────────────
diff --git a/tests/test_sprint46.py b/tests/test_sprint46.py
index 272f86689..9ca5bed66 100644
--- a/tests/test_sprint46.py
+++ b/tests/test_sprint46.py
@@ -129,6 +129,178 @@ def test_session_compress_requires_session_id(cleanup_test_sessions):
     assert handler.payload()["error"] == "Missing required field(s): session_id"
 
 
+def test_session_compress_stale_runtime_returns_typed_409_before_mutation(
+    monkeypatch, cleanup_test_sessions
+):
+    import api.routes as routes
+
+    sid = _make_session()
+    cleanup_test_sessions.append(sid)
+    loaded_before = Session.load(sid)
+    assert loaded_before is not None
+    before = loaded_before.compact()
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+
+    handler = _FakeHandler()
+    _handle_session_compress(handler, {"session_id": sid})
+
+    assert handler.status == 409
+    assert handler.payload() == {
+        "error": "restart required",
+        "type": "agent_runtime_stale",
+        "retryable": True,
+    }
+    loaded_after = Session.load(sid)
+    assert loaded_after is not None
+    assert loaded_after.compact() == before
+
+
+def test_session_compress_start_stale_runtime_returns_409_before_job_creation(
+    monkeypatch, cleanup_test_sessions
+):
+    import api.routes as routes
+
+    sid = _make_session()
+    cleanup_test_sessions.append(sid)
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        routes._MANUAL_COMPRESSION_JOBS.pop(sid, None)
+
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+
+    handler = _FakeHandler()
+    routes._handle_session_compress_start(handler, {"session_id": sid})
+
+    assert handler.status == 409
+    assert json.loads(handler.wfile.getvalue().decode("utf-8")) == {
+        "error": "restart required",
+        "type": "agent_runtime_stale",
+        "retryable": True,
+    }
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        assert sid not in routes._MANUAL_COMPRESSION_JOBS
+
+
+def test_session_compress_start_reuses_running_job_when_runtime_is_stale(
+    monkeypatch, cleanup_test_sessions
+):
+    import api.routes as routes
+
+    sid = _make_session()
+    cleanup_test_sessions.append(sid)
+    existing = {
+        "session_id": sid,
+        "focus_topic": "already running",
+        "status": "running",
+        "started_at": time.time(),
+        "updated_at": time.time(),
+    }
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        routes._MANUAL_COMPRESSION_JOBS[sid] = existing
+    monkeypatch.setattr(
+        routes,
+        "ensure_agent_runtime_current",
+        lambda: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+
+    handler = _FakeHandler()
+    routes._handle_session_compress_start(handler, {"session_id": sid})
+
+    assert handler.status == 200
+    payload = handler.payload()
+    assert payload["status"] == "running"
+    assert payload["session_id"] == sid
+    assert payload["focus_topic"] == "already running"
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        assert routes._MANUAL_COMPRESSION_JOBS[sid] is existing
+        routes._MANUAL_COMPRESSION_JOBS.pop(sid, None)
+
+
+def test_session_compress_start_rechecks_job_after_runtime_barrier(
+    monkeypatch, cleanup_test_sessions
+):
+    import api.routes as routes
+
+    sid = _make_session()
+    cleanup_test_sessions.append(sid)
+    admitted = {
+        "session_id": sid,
+        "focus_topic": "admitted concurrently",
+        "status": "running",
+        "started_at": time.time(),
+        "updated_at": time.time(),
+    }
+
+    def barrier_then_admit():
+        with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+            routes._MANUAL_COMPRESSION_JOBS[sid] = admitted
+
+    def reject_duplicate_worker(**_kwargs):
+        raise AssertionError("duplicate worker admitted")
+
+    monkeypatch.setattr(routes, "ensure_agent_runtime_current", barrier_then_admit)
+    monkeypatch.setattr(routes.threading, "Thread", reject_duplicate_worker)
+
+    handler = _FakeHandler()
+    routes._handle_session_compress_start(handler, {"session_id": sid})
+
+    assert handler.status == 200
+    assert handler.payload()["status"] == "running"
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        routes._MANUAL_COMPRESSION_JOBS.pop(sid, None)
+
+
+def test_session_compress_worker_preserves_stale_runtime_taxonomy(monkeypatch):
+    import api.routes as routes
+
+    sid = "stale-worker-session"
+    started_at = time.time()
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        routes._MANUAL_COMPRESSION_JOBS[sid] = {
+            "session_id": sid,
+            "status": "running",
+            "started_at": started_at,
+            "updated_at": started_at,
+        }
+
+    monkeypatch.setattr(
+        routes,
+        "_handle_session_compress",
+        lambda *_args, **_kwargs: (_ for _ in ()).throw(
+            routes.AgentRuntimeChangedError("restart required")
+        ),
+    )
+
+    routes._run_manual_compression_job(sid, {"session_id": sid})
+
+    handler = _FakeHandler()
+    routes._handle_session_compress_status(handler, sid)
+    payload = handler.payload()
+    assert handler.status == 200
+    assert payload["ok"] is False
+    assert payload["status"] == "error"
+    assert payload["session_id"] == sid
+    assert payload["error"] == "restart required"
+    assert payload["error_status"] == 409
+    assert payload["type"] == "agent_runtime_stale"
+    assert payload["retryable"] is True
+    with routes._MANUAL_COMPRESSION_JOBS_LOCK:
+        routes._MANUAL_COMPRESSION_JOBS.pop(sid, None)
+
+
 def test_session_compress_roundtrip(monkeypatch, cleanup_test_sessions):
     created = cleanup_test_sessions
     original_messages = [
diff --git a/tests/test_update_banner_fixes.py b/tests/test_update_banner_fixes.py
index 0ab7a0518..0da5ad417 100644
--- a/tests/test_update_banner_fixes.py
+++ b/tests/test_update_banner_fixes.py
@@ -1635,7 +1635,7 @@ class TestUpdateSummaryRouteModelSelection:
         assert '"update_summary"' not in src
         assert 'main_runtime=main_runtime' in src
         assert 'update summary auxiliary model failed; falling back to main model' in src
-        assert 'from run_agent import AIAgent' in src
+        assert 'require_ai_agent_class()' in src
 
     def test_summary_route_auxiliary_model_uses_active_profile_env(self, monkeypatch, tmp_path):
         import api.config as cfg
diff --git a/tests/test_v050259_sessiondb_fd_leak.py b/tests/test_v050259_sessiondb_fd_leak.py
index 3b80ac974..12bfd90e4 100644
--- a/tests/test_v050259_sessiondb_fd_leak.py
+++ b/tests/test_v050259_sessiondb_fd_leak.py
@@ -1,18 +1,25 @@
-"""Regression tests for v0.50.259 — SessionDB FD leak fixes from PR #1421
-plus Opus pre-release advisor follow-up extending the fix to LRU eviction.
+"""Regression tests for SessionDB FD-leak fixes (PR #1421) plus the
+subagent shared-handle race (close-under-live-subagents).
 
-The bug: `_run_agent_streaming` created a new `SessionDB` per request and
+History
+-------
+PR #1421: `_run_agent_streaming` created a new `SessionDB` per request and
 replaced the cached agent's `_session_db` without closing the old one.
 After ~73 messages on a long-lived agent, leaked FDs exhausted the 256 FD
-default limit causing `EMFILE` crashes.
+default limit causing `EMFILE` crashes. Fix: close the previous handle
+when it is safe to replace it.
 
-Fix path 1 (PR #1421 by @wali-reheman): close `agent._session_db` before
-replacing it on the cached-agent reuse path.
+Follow-up (this change): always-close-before-replace is *not* safe when
+background subagents still hold a reference to the same SessionDB object
+(delegate_tool copies ``parent._session_db`` by ref). A server-side wakeup
+/ new turn for the parent session was closing the shared handle mid-child-
+run, producing:
 
-Fix path 2 (this PR Opus follow-up): same shape on the LRU eviction path.
-When `SESSION_AGENT_CACHE.popitem(last=False)` evicts an old agent, its
-`_session_db` is dropped on the floor and only released when GC eventually
-finalizes the agent — which on a long-running server may be never.
+    Session DB append_message failed: 'NoneType' object has no attribute 'execute'
+
+Policy now (``_adopt_session_db_for_cached_agent``):
+- existing handle still open → keep it, close the unused *new* handle
+- existing handle missing/closed → adopt the new handle (close dead one)
 """
 
 from __future__ import annotations
@@ -25,38 +32,56 @@ import pytest
 REPO = Path(__file__).resolve().parents[1]
 
 
-# ── 1: source-level pin: cached-agent-reuse path closes _session_db ─────────
+# ── 1: source-level pin: cached-agent reuse uses the adopt helper ──────────
 
 
-def test_cached_agent_reuse_closes_old_session_db():
-    """The cached-agent reuse path in `_run_agent_streaming` MUST close the
-    old `_session_db` before replacing it. Without this, every streaming
-    request leaks a SessionDB connection (3 FDs once WAL is active)."""
+def test_cached_agent_reuse_uses_adopt_helper():
+    """Cached-agent reuse must go through `_adopt_session_db_for_cached_agent`
+    so a still-open SessionDB is reused (subagent-safe) and only a dead handle
+    is closed+replaced (still EMFILE-safe)."""
     src = (REPO / "api" / "streaming.py").read_text(encoding="utf-8")
 
-    # Find the cached-agent reuse block (where callbacks are refreshed).
-    # The replacement of agent._session_db must be preceded by a close().
     reuse_idx = src.find("Refresh per-turn callbacks")
     assert reuse_idx != -1, "cached-agent reuse block missing"
     block = src[reuse_idx : reuse_idx + 2500]
 
-    # Must close before replace.
-    assert "agent._session_db.close()" in block, (
-        "cached-agent reuse path must call agent._session_db.close() before "
-        "replacing it. Without this, FDs leak on every streaming request "
-        "and the server EMFILE-crashes after ~73 messages. See PR #1421."
+    assert "_adopt_session_db_for_cached_agent" in block, (
+        "cached-agent reuse path must call _adopt_session_db_for_cached_agent "
+        "instead of unconditionally closing agent._session_db. Unconditional "
+        "close breaks background subagents that share the handle by reference."
     )
-    # And the close must come BEFORE the replacement (lexically).
-    close_idx = block.find("agent._session_db.close()")
-    replace_idx = block.find("agent._session_db = _session_db")
-    assert close_idx != -1 and replace_idx != -1
-    assert close_idx < replace_idx, (
-        "close() must lexically precede the assignment so the old connection "
-        "is released before the reference is rebound."
+    assert "agent._session_db = _session_db" in block, (
+        "reuse path must still assign the adopted SessionDB onto the agent"
+    )
+    # The old unconditional-close pattern must not remain in the reuse block.
+    assert "agent._session_db.close()" not in block, (
+        "unconditional agent._session_db.close() in the reuse path is the "
+        "subagent race; close is now owned by _adopt_session_db_for_cached_agent"
     )
 
 
-# ── 2: source-level pin: LRU eviction path also closes _session_db ──────────
+def test_adopt_and_is_open_helpers_exist():
+    src = (REPO / "api" / "streaming.py").read_text(encoding="utf-8")
+    assert "def _session_db_is_open(" in src
+    assert "def _adopt_session_db_for_cached_agent(" in src
+    # self-heal path must also refuse to close a still-open handle
+    replace_idx = src.find("def _replace_session_db_in_kwargs")
+    assert replace_idx != -1
+    block = src[replace_idx : replace_idx + 1200]
+    assert "_session_db_is_open" in block, (
+        "_replace_session_db_in_kwargs must guard on _session_db_is_open so "
+        "credential self-heal cannot close a handle live subagents share"
+    )
+    # adopt helper must log failed closes (not bare `pass`) so EMFILE pressure
+    # from a failed close is diagnosable — matches _replace_session_db_in_kwargs.
+    adopt_idx = src.find("def _adopt_session_db_for_cached_agent")
+    assert adopt_idx != -1
+    adopt_block = src[adopt_idx : adopt_idx + 1800]
+    assert 'Failed to close unused session_db handle in adopt helper' in adopt_block
+    assert "logger.debug" in adopt_block
+
+
+# ── 2: source-level pin: LRU eviction path still closes _session_db ────────
 
 
 def test_lru_eviction_closes_evicted_agent_session_db():
@@ -66,27 +91,21 @@ def test_lru_eviction_closes_evicted_agent_session_db():
     on GC finalization which may never run on a long-lived server.
 
     Fix: capture the evicted entry, close its agent's `_session_db` before
-    dropping the reference.
+    dropping the reference. (Eviction is a true session boundary — no live
+    subagents are expected to still be writing into that agent.)
     """
     src = (REPO / "api" / "streaming.py").read_text(encoding="utf-8")
 
-    # The eviction site uses popitem(last=False). The evicted entry must be
-    # captured (not discarded with `_`) and the agent's _session_db closed.
     eviction_idx = src.find("Evicted LRU agent from cache")
     assert eviction_idx != -1, "LRU eviction debug log missing"
-    # Look in a window around the eviction.
     block = src[max(0, eviction_idx - 1500) : eviction_idx + 200]
 
-    # Negative pattern: the old `evicted_sid, _ = ...` discard form must NOT
-    # be present — that's the bug shape.
     assert "evicted_sid, _ = SESSION_AGENT_CACHE.popitem" not in block, (
-        "LRU eviction must capture the evicted entry so the agent\'s "
+        "LRU eviction must capture the evicted entry so the agent's "
         "_session_db can be closed. The `evicted_sid, _ = ...` discard form "
         "is the original bug shape."
     )
 
-    # Positive pattern: eviction must call the lifecycle helper, and the helper
-    # must close the evicted agent's SessionDB after provider teardown.
     assert "_close_evicted_agent_at_session_boundary(_evicted_sid, _evicted_agent)" in block, (
         "LRU eviction must route the evicted agent through the session-boundary "
         "close helper."
@@ -104,16 +123,7 @@ def test_lru_eviction_closes_evicted_agent_session_db():
 
 
 def test_session_db_close_is_idempotent():
-    """`SessionDB.close()` must be safe to call multiple times. The fix
-    relies on this — if a future code path closes the same `_session_db`
-    after we've swapped it, the second close is a benign no-op.
-
-    Skipped when hermes_state is not on the import path (e.g. on the GH
-    Actions runner that only has the WebUI repo, not the agent repo).
-    The source-level pin in test_cached_agent_reuse_closes_old_session_db
-    catches revert of the close() call; this test only adds runtime
-    confirmation when both repos are co-located.
-    """
+    """`SessionDB.close()` must be safe to call multiple times."""
     import importlib.util
     if importlib.util.find_spec("hermes_state") is None:
         pytest.skip("hermes_state not on import path (CI-only — agent repo not present)")
@@ -123,65 +133,123 @@ def test_session_db_close_is_idempotent():
     with tempfile.TemporaryDirectory() as tmpd:
         db_path = Path(tmpd) / "test.db"
         db = SessionDB(db_path=db_path)
-        # Force connection open by issuing a query.
         with db._lock:
             db._conn.execute("SELECT 1")
-        # First close
         db.close()
         assert db._conn is None
-        # Second close — must not raise.
         db.close()
         assert db._conn is None
-        # Third close — still safe.
         db.close()
 
 
-# ── 4: behavioral: cached-agent reuse with mock agent ───────────────────────
+# ── 4: behavioral: adopt helper keeps open handles, closes dead ones ───────
 
 
-def test_cached_agent_reuse_calls_close_on_old_session_db():
-    """End-to-end: simulate the cached-agent reuse code path with a mock
-    agent and verify the mock SessionDB.close() is called when _session_db
-    is replaced. Pins the runtime behavior, not just the source pattern."""
-    import sys
-    sys.path.insert(0, str(REPO))
+class _MockSessionDB:
+    def __init__(self, name, open_=True):
+        self.name = name
+        self.close_calls = 0
+        # Mirror SessionDB: open → _conn is truthy; closed → _conn is None.
+        self._conn = object() if open_ else None
 
-    class MockSessionDB:
-        def __init__(self, name):
-            self.name = name
-            self.close_calls = 0
-        def close(self):
-            self.close_calls += 1
+    def close(self):
+        self.close_calls += 1
+        self._conn = None
 
-    class MockAgent:
-        def __init__(self, db):
-            self._session_db = db
-            self.stream_delta_callback = None
-            self.tool_progress_callback = None
-            self._api_call_count = 0
-            self._interrupted = False
-            self._interrupt_message = None
 
-    # Simulate the inner block of the cached-agent reuse path. We replicate
-    # the pattern manually rather than importing _run_agent_streaming
-    # directly because that function has many other side effects.
-    old_db = MockSessionDB("old")
-    new_db = MockSessionDB("new")
-    agent = MockAgent(old_db)
+class _MockAgent:
+    def __init__(self, db):
+        self._session_db = db
+        self.stream_delta_callback = None
+        self.tool_progress_callback = None
+        self._api_call_count = 0
+        self._interrupted = False
+        self._interrupt_message = None
 
-    # Mirror the production code path:
-    if hasattr(agent, "_session_db") and agent._session_db is not None:
-        try:
-            agent._session_db.close()
-        except Exception:
-            pass
-    agent._session_db = new_db
 
-    assert old_db.close_calls == 1, (
-        "old SessionDB must be closed exactly once when replaced on cached agent"
-    )
-    assert new_db.close_calls == 0, "new SessionDB should not be closed"
+def _import_adopt_helpers():
+    """Import the production helpers.
+
+    No source-slicing / exec fallback: that path breaks as soon as the helpers
+    reference module-level names (e.g. ``logger.debug``) or another def is
+    inserted between the markers. Prefer a real import; skip the behavioral
+    suite when the package cannot be imported (CI without full deps).
+    Source-level pins above still catch reverts without importing streaming.
+    """
+    try:
+        from api.streaming import (  # type: ignore
+            _adopt_session_db_for_cached_agent,
+            _session_db_is_open,
+        )
+    except Exception as exc:
+        pytest.skip(f"api.streaming helpers not importable: {exc}")
+    return _session_db_is_open, _adopt_session_db_for_cached_agent
+
+
+def test_adopt_reuses_open_session_db_and_closes_new():
+    """Live (open) existing handle must be kept; unused new handle closed.
+
+    This is the subagent-safe path: children hold a reference to `old_db`.
+    """
+    _is_open, adopt = _import_adopt_helpers()
+    old_db = _MockSessionDB("old", open_=True)
+    new_db = _MockSessionDB("new", open_=True)
+    agent = _MockAgent(old_db)
+
+    result = adopt(agent, new_db)
+
+    assert result is old_db
+    assert agent._session_db is old_db
+    assert old_db.close_calls == 0, "must not close the live shared handle"
+    assert new_db.close_calls == 1, "unused per-request handle must be closed (FD leak)"
+    assert _is_open(old_db) is True
+    assert _is_open(new_db) is False
+
+
+def test_adopt_replaces_closed_session_db():
+    """Dead existing handle is closed (idempotent) and replaced with the new one."""
+    _is_open, adopt = _import_adopt_helpers()
+    old_db = _MockSessionDB("old", open_=False)
+    new_db = _MockSessionDB("new", open_=True)
+    agent = _MockAgent(old_db)
+
+    result = adopt(agent, new_db)
+
+    assert result is new_db
     assert agent._session_db is new_db
+    assert old_db.close_calls == 1
+    assert new_db.close_calls == 0
+
+
+def test_adopt_handles_missing_existing():
+    _is_open, adopt = _import_adopt_helpers()
+    new_db = _MockSessionDB("new", open_=True)
+    agent = _MockAgent(None)
+    agent._session_db = None
+
+    result = adopt(agent, new_db)
+
+    assert result is new_db
+    assert agent._session_db is new_db
+    assert new_db.close_calls == 0
+
+
+def test_cached_agent_reuse_calls_adopt_semantics():
+    """End-to-end mirror of the production reuse block using the real helper."""
+    _is_open, adopt = _import_adopt_helpers()
+    old_db = _MockSessionDB("old", open_=True)
+    new_db = _MockSessionDB("new", open_=True)
+    agent = _MockAgent(old_db)
+    _session_db = new_db
+
+    # Mirror production:
+    if _session_db is not None:
+        _session_db = adopt(agent, _session_db)
+        agent._session_db = _session_db
+
+    assert agent._session_db is old_db
+    assert old_db.close_calls == 0
+    assert new_db.close_calls == 1
 
 
 # ── 5: behavioral: LRU eviction with mock agents ────────────────────────────
@@ -192,24 +260,12 @@ def test_lru_eviction_closes_evicted_session_db():
     SessionDB.close() is called."""
     import collections
 
-    class MockSessionDB:
-        def __init__(self, name):
-            self.name = name
-            self.close_calls = 0
-        def close(self):
-            self.close_calls += 1
-
-    class MockAgent:
-        def __init__(self, db):
-            self._session_db = db
-
     cache = collections.OrderedDict()
-    db1, db2, db3 = MockSessionDB("a"), MockSessionDB("b"), MockSessionDB("c")
-    cache["sid-a"] = (MockAgent(db1), "sig1")
-    cache["sid-b"] = (MockAgent(db2), "sig2")
-    cache["sid-c"] = (MockAgent(db3), "sig3")
+    db1, db2, db3 = _MockSessionDB("a"), _MockSessionDB("b"), _MockSessionDB("c")
+    cache["sid-a"] = (_MockAgent(db1), "sig1")
+    cache["sid-b"] = (_MockAgent(db2), "sig2")
+    cache["sid-c"] = (_MockAgent(db3), "sig3")
 
-    # Mirror the production eviction path with MAX=2:
     MAX = 2
     while len(cache) > MAX:
         evicted_sid, evicted_entry = cache.popitem(last=False)
@@ -220,8 +276,59 @@ def test_lru_eviction_closes_evicted_session_db():
         except Exception:
             pass
 
-    # First-inserted entry (sid-a) was evicted.
     assert "sid-a" not in cache
     assert db1.close_calls == 1, "evicted agent's SessionDB must be closed exactly once"
     assert db2.close_calls == 0, "remaining agents' SessionDBs must not be touched"
     assert db3.close_calls == 0
+
+
+# ── 6: self-heal path must not reuse a CLOSED handle when the rebuild fails ──
+
+
+def _import_replace_helper():
+    """Import the real credential-self-heal SessionDB replacer."""
+    try:
+        from api.streaming import _replace_session_db_in_kwargs  # type: ignore
+    except Exception as exc:
+        pytest.skip(f"api.streaming not importable: {exc}")
+    return _replace_session_db_in_kwargs
+
+
+def test_replace_degrades_to_none_when_rebuild_fails_and_old_is_closed(monkeypatch):
+    """Credential self-heal regression (Codex gate finding on PR #6143).
+
+    When ``_build_session_db_for_stream`` returns None (rebuild failed) AND the
+    prior handle is already CLOSED, ``_replace_session_db_in_kwargs`` must leave
+    ``agent_kwargs['session_db'] = None`` — as master did — so the rebuilt agent
+    lazily reinitialises. Retaining the closed handle (the pre-fix behaviour)
+    makes every persist/search fail with
+    ``'NoneType' object has no attribute 'execute'`` while the chat continues.
+    """
+    import api.streaming as streaming
+
+    _replace = _import_replace_helper()
+    monkeypatch.setattr(streaming, "_build_session_db_for_stream", lambda _p: None)
+
+    old_db = _MockSessionDB("old", open_=False)  # already closed
+    kwargs = {"session_db": old_db}
+    result = _replace(kwargs, "/tmp/does-not-matter.db")
+
+    assert result is None, "must not hand back a closed handle when rebuild fails"
+    assert kwargs["session_db"] is None, "kwargs must degrade to None (clean lazy reinit)"
+
+
+def test_replace_keeps_open_handle_when_rebuild_fails(monkeypatch):
+    """Inverse: a still-OPEN prior handle (held by live subagents) is retained
+    when the rebuild fails — do not orphan a live shared connection."""
+    import api.streaming as streaming
+
+    _replace = _import_replace_helper()
+    monkeypatch.setattr(streaming, "_build_session_db_for_stream", lambda _p: None)
+
+    old_db = _MockSessionDB("old", open_=True)  # still live (subagents hold it)
+    kwargs = {"session_db": old_db}
+    result = _replace(kwargs, "/tmp/does-not-matter.db")
+
+    assert result is old_db, "a live handle must be kept when the rebuild fails"
+    assert kwargs["session_db"] is old_db
+    assert old_db.close_calls == 0, "must not close a live shared handle"