diff --git a/gateway/run_shutdown.py b/gateway/run_shutdown.py
index 52bf07449a..dcd93ff693 100644
--- a/gateway/run_shutdown.py
+++ b/gateway/run_shutdown.py
@@ -1055,16 +1055,17 @@ class GatewayShutdownMixin:
                 flush_agent_history_to_file(getattr(agent, "session_id", None), _session_messages)
 
     async def _finalize_shutdown_agents(self, active_agents: Dict[str, Any]) -> None:
-        for agent in active_agents.values():
+        for session_key, agent in active_agents.items():
             self._flush_agent_transcript_at_shutdown(agent)
             # Off-loop + bounded: plugin on_session_finalize hooks can do arbitrary synchronous work
             # (e.g. a full-session trace export) — same hang class as the memory provider below.
             await self._finalize_session_off_loop(
                 session_id=getattr(agent, "session_id", None), platform="gateway", reason="shutdown",
+                session_key=session_key,
             )
             # Off-loop + bounded: a wedged memory provider here used to hang the whole shutdown so
             # SIGTERM never completed.
-            await self._cleanup_agent_resources_off_loop(agent, context="shutdown finalize")
+            await self._cleanup_agent_resources_off_loop(agent, context="shutdown finalize", session_key=session_key)
 
     def _should_emit_long_running_notification(
         self, session_key: Optional[str], agent: Any, executor_task: Optional[Any],
@@ -1109,15 +1110,23 @@ class GatewayShutdownMixin:
             tasks = self._deferred_agent_cleanup_tasks = set()
         self._track_task_in(tasks, asyncio.create_task(_cleanup_when_done()))
 
-    async def _finalize_session_off_loop(self, *, session_id: Any, platform: str, reason: str, **extra: Any) -> None:
-        """Run hermes_cli.lifecycle.finalize_session off-loop, bounded; on timeout the worker is left alone."""
+    async def _finalize_session_off_loop(
+        self, *, session_id: Any, platform: str, reason: str, session_key: Optional[str] = None, **extra: Any,
+    ) -> None:
+        """Run hermes_cli.lifecycle.finalize_session off-loop, bounded; on timeout the worker is left alone.
+        ``session_key`` lets an unscoped caller (shutdown) enter the owning profile's scope: plugin
+        ``on_session_finalize`` observers and the Relay coordinator (``current_profile_key``) resolve
+        profile state at call time."""
 
         def _call() -> None:
             from hermes_cli.lifecycle import finalize_session
             finalize_session(session_id=session_id, platform=platform, reason=reason, **extra)
 
         try:
-            await asyncio.wait_for(self._run_in_executor_with_context(_call), timeout=self._FINALIZE_TIMEOUT_S)
+            await asyncio.wait_for(
+                self._run_in_executor_with_context(self._run_release_in_profile_scope, _call, (), session_key),
+                timeout=self._FINALIZE_TIMEOUT_S,
+            )
         except asyncio.TimeoutError:
             logger.warning(
                 "Session finalize hooks (%s, reason=%s) exceeded %ss; proceeding without blocking the event loop "
@@ -1126,8 +1135,17 @@ class GatewayShutdownMixin:
         except Exception as finalize_exc:
             logger.debug("Session finalize hooks (%s, reason=%s) failed: %s", session_id, reason, finalize_exc)
 
-    async def _cleanup_agent_resources_off_loop(self, agent: Any, *, context: str = "") -> None:
-        """Run _cleanup_agent_resources in a worker thread, bounded; on timeout the worker is left alone."""
+    async def _cleanup_agent_resources_off_loop(
+        self, agent: Any, *, context: str = "", session_key: Optional[str] = None,
+    ) -> None:
+        """Run _cleanup_agent_resources in a worker thread, bounded; on timeout the worker is left alone.
+
+        The teardown fires the memory-provider lifecycle hooks (``flush_pending`` → ``on_session_end`` →
+        ``shutdown`` → ``close``), which read credentials/home at call time. In-turn callers carry the
+        profile scope through ``_run_in_executor_with_context``; shutdown does not (it runs on the main
+        loop, outside any adapter handler), so under multiplexing ``on_session_end`` failed closed and the
+        session tail was never committed (#110622). ``_run_release_in_profile_scope`` enters the OWNING
+        profile's scope from ``session_key`` when the caller has none, exactly like cache eviction."""
         if agent is None:
             return
         if context.startswith("shutdown") or context == "session expiry":
@@ -1136,7 +1154,9 @@ class GatewayShutdownMixin:
         ctx_label = f" ({context})" if context else ""
         try:
             await asyncio.wait_for(
-                self._run_in_executor_with_context(self._cleanup_agent_resources, agent),
+                self._run_in_executor_with_context(
+                    self._run_release_in_profile_scope, self._cleanup_agent_resources, (agent,), session_key,
+                ),
                 timeout=self._CLEANUP_TIMEOUT_S,
             )
         except asyncio.TimeoutError:
@@ -1717,12 +1737,13 @@ class GatewayShutdownMixin:
         _cache = getattr(self, "_agent_cache", None)
         if _cache_lock is not None and _cache is not None:
             with _cache_lock:
-                _idle_agents = list(_cache.values())
+                _idle_agents = list(_cache.items())
                 _cache.clear()
-            for _entry in _idle_agents:
+            for _key, _entry in _idle_agents:
                 # Bounded + off-loop: a wedged memory provider here once made SIGTERM hang forever.
                 await self._cleanup_agent_resources_off_loop(
-                    _entry[0] if isinstance(_entry, tuple) else _entry, context="shutdown idle-cache"
+                    _entry[0] if isinstance(_entry, tuple) else _entry, context="shutdown idle-cache",
+                    session_key=_key,
                 )
         # Settle completion flush tasks while adapters are alive so every watcher gets a retryable result.
         cancel_completion_batches = getattr(self, "_cancel_process_completion_batch_tasks", None)
diff --git a/tests/gateway/test_finalize_session_off_loop.py b/tests/gateway/test_finalize_session_off_loop.py
index cf10d13617..e209ebae9c 100644
--- a/tests/gateway/test_finalize_session_off_loop.py
+++ b/tests/gateway/test_finalize_session_off_loop.py
@@ -133,7 +133,7 @@ def test_shutdown_finalize_path_uses_off_loop_dispatch(monkeypatch):
         GatewayRunner, "_finalize_session_off_loop", _fake_off_loop
     )
 
-    async def _fake_cleanup(self, agent, *, context=""):
+    async def _fake_cleanup(self, agent, *, context="", session_key=None):
         return None
 
     monkeypatch.setattr(
diff --git a/tests/gateway/test_shutdown_cache_cleanup.py b/tests/gateway/test_shutdown_cache_cleanup.py
index 71b77e47a4..3123bb825f 100644
--- a/tests/gateway/test_shutdown_cache_cleanup.py
+++ b/tests/gateway/test_shutdown_cache_cleanup.py
@@ -76,7 +76,7 @@ class _FakeGateway:
         # inline in tests so the bounded-cleanup path is exercised.
         return func(*args)
 
-    async def _cleanup_agent_resources_off_loop(self, agent, *, context=""):
+    async def _cleanup_agent_resources_off_loop(self, agent, *, context="", session_key=None):
         # Mirror the real bounded helper, inline (no executor/timeout) so the
         # fake exercises the same call shape stop() now uses.
         self._cleanup_agent_resources(agent)
diff --git a/tests/gateway/test_shutdown_teardown_profile_scope.py b/tests/gateway/test_shutdown_teardown_profile_scope.py
new file mode 100644
index 0000000000..c44a4eb76d
--- /dev/null
+++ b/tests/gateway/test_shutdown_teardown_profile_scope.py
@@ -0,0 +1,88 @@
+"""Multiplex invariant: gateway-hosted teardown fires memory-provider lifecycle hooks under the
+OWNING profile's scope (#110622).
+
+``on_session_end`` / ``shutdown`` / ``close`` read credentials and home at call time. Shutdown
+runs on the main loop outside any adapter handler, so its executor hop carried an EMPTY scope and
+a secondary profile's ``get_secret("OPENVIKING_API_KEY")`` failed closed — the end-of-session
+commit was skipped and logged as a WARNING + traceback on every gateway-hosted session close.
+"""
+from __future__ import annotations
+
+import asyncio
+from contextvars import copy_context
+from pathlib import Path
+from types import SimpleNamespace
+
+import pytest
+
+from agent import secret_scope
+from gateway.config import GatewayConfig
+from gateway.run import GatewayRunner
+from hermes_constants import get_hermes_home
+
+
+def _runner(profile_homes: dict[str, Path]) -> GatewayRunner:
+    runner = object.__new__(GatewayRunner)
+    runner.config = GatewayConfig(multiplex_profiles=True)
+    runner.session_store = SimpleNamespace(_profile_home_for_key=lambda key: profile_homes.get(key))
+    from concurrent.futures import ThreadPoolExecutor
+    executor = ThreadPoolExecutor(max_workers=2)
+
+    async def _run_in_executor_with_context(func, *args):
+        loop = asyncio.get_running_loop()
+        ctx = copy_context()
+        return await loop.run_in_executor(executor, lambda: ctx.run(func, *args))
+
+    runner._run_in_executor_with_context = _run_in_executor_with_context
+    return runner
+
+
+def _recording_agent(seen: dict):
+    class _Provider:
+        name = "recorder"
+
+        def on_session_end(self, messages):
+            seen["scope"] = secret_scope.current_secret_scope()
+            seen["home"] = get_hermes_home()
+
+    def shutdown_memory_provider(messages=None):
+        _Provider().on_session_end(messages)
+
+    return SimpleNamespace(
+        shutdown_memory_provider=shutdown_memory_provider, close=lambda: None, _session_messages=[],
+    )
+
+
+@pytest.mark.asyncio
+async def test_shutdown_teardown_commits_memory_under_the_owning_profile(tmp_path, monkeypatch):
+    default_home = tmp_path / ".hermes"
+    prof_b = default_home / "profiles" / "b"
+    prof_b.mkdir(parents=True)
+    (prof_b / ".env").write_text("OPENVIKING_API_KEY=key-of-b\n")
+    monkeypatch.setenv("HERMES_HOME", str(default_home))
+    seen: dict = {}
+    secret_scope.set_multiplex_active(True)
+    try:
+        # Shutdown runs on the main loop with NO scope installed.
+        assert secret_scope.current_secret_scope() is None
+        await _runner({"agent:b:telegram:dm:1": prof_b})._cleanup_agent_resources_off_loop(
+            _recording_agent(seen), context="shutdown finalize", session_key="agent:b:telegram:dm:1",
+        )
+    finally:
+        secret_scope.set_multiplex_active(False)
+    assert seen["home"] == prof_b
+    assert seen["scope"] and seen["scope"].get("OPENVIKING_API_KEY") == "key-of-b"
+
+
+@pytest.mark.asyncio
+async def test_in_turn_teardown_keeps_the_callers_scope(tmp_path, monkeypatch):
+    monkeypatch.setenv("HERMES_HOME", str(tmp_path))
+    seen: dict = {}
+    secret_scope.set_multiplex_active(True)
+    token = secret_scope.set_secret_scope({"MARKER": "turn-scope"})
+    try:
+        await _runner({})._cleanup_agent_resources_off_loop(_recording_agent(seen), context="session hygiene")
+    finally:
+        secret_scope.reset_secret_scope(token)
+        secret_scope.set_multiplex_active(False)
+    assert seen["scope"] == {"MARKER": "turn-scope"}