diff --git a/gateway/run.py b/gateway/run.py
index f105d27a251..0145089b940 100644
--- a/gateway/run.py
+++ b/gateway/run.py
@@ -4674,6 +4674,40 @@ class GatewayRunner(GatewayAuthorizationMixin, GatewayKanbanWatchersMixin, Gatew
 
     def _finalize_shutdown_agents(self, active_agents: Dict[str, Any]) -> None:
         for agent in active_agents.values():
+            # Persist any in-flight transcript to the SQLite session store
+            # before teardown (#13121).  An agent forcibly interrupted by the
+            # drain-timeout escalation may never reach
+            # ``turn_finalizer.finalize_turn`` (the only place that flushes the
+            # turn to state.db) — e.g. it was blocked in a tool call that did
+            # not abort within the post-interrupt grace window.  Its in-flight
+            # tool rounds live only in the in-memory ``_session_messages``
+            # (refreshed per tool round in ``conversation_loop`` but never
+            # written to SQLite mid-turn), so the immediate pre-restart turn is
+            # silently dropped from ``load_transcript()`` on resume.  Flushing
+            # here closes that gap; the resume_pending / fresh-tool-tail
+            # branches in ``_handle_message_with_agent`` already expect a
+            # transcript whose tail may be a pending tool result.  The flush is
+            # idempotent (identity-tracked in ``_flush_messages_to_session_db``),
+            # so agents that DID finish gracefully re-flush nothing.
+            try:
+                _flush = getattr(agent, "_flush_messages_to_session_db", None)
+                _session_messages = getattr(agent, "_session_messages", None)
+                if callable(_flush) and isinstance(_session_messages, list) and _session_messages:
+                    # Strip private empty-response retry scaffolding from the
+                    # tail first, mirroring the graceful ``_persist_session``
+                    # path, so a resumed turn doesn't replay synthetic recovery
+                    # nudges.
+                    _strip = getattr(
+                        agent, "_drop_trailing_empty_response_scaffolding", None
+                    )
+                    if callable(_strip):
+                        try:
+                            _strip(_session_messages)
+                        except Exception:
+                            pass
+                    _flush(_session_messages)
+            except Exception as _e:
+                logger.debug("Shutdown transcript flush failed: %s", _e)
             try:
                 from hermes_cli.plugins import invoke_hook as _invoke_hook
                 _invoke_hook(
diff --git a/tests/gateway/test_13121_shutdown_inflight_transcript_flush.py b/tests/gateway/test_13121_shutdown_inflight_transcript_flush.py
new file mode 100644
index 00000000000..d726ea34352
--- /dev/null
+++ b/tests/gateway/test_13121_shutdown_inflight_transcript_flush.py
@@ -0,0 +1,243 @@
+"""Regression tests for #13121 — gateway restart/shutdown must persist an
+in-flight (interrupted) turn's transcript to the SQLite session store so the
+immediate pre-restart context survives ``load_transcript()`` on resume.
+
+The bug: every normal/graceful turn exit funnels through
+``turn_finalizer.finalize_turn`` which calls ``_persist_session`` →
+``_flush_messages_to_session_db`` (the only place a turn is written to
+state.db).  During the tool loop only the *in-memory* ``_session_messages``
+reference is refreshed per round — there is no incremental SQLite flush
+mid-turn.
+
+When the gateway drain times out it marks the session ``resume_pending``,
+interrupts the running agents, waits a short grace window, then tears them
+down via ``_finalize_shutdown_agents`` → ``_cleanup_agent_resources``.  An
+agent blocked in a tool call that does not abort within the grace window
+never reaches ``finalize_turn``, so its in-flight tool rounds live only in
+``_session_messages`` and are never written to state.db.  On resume,
+``load_transcript()`` (state.db is now the canonical store — the legacy
+JSONL fallback was dropped) returns the pre-turn state, dropping the
+immediate pre-restart turn.
+
+The fix flushes ``_session_messages`` to the session DB in
+``_finalize_shutdown_agents`` before teardown.  The flush is idempotent
+(identity-tracked in ``_flush_messages_to_session_db``), so agents that DID
+finish gracefully re-flush nothing.
+
+These tests exercise BOTH a lightweight unit path (the flush hook is invoked
+with the in-flight messages) AND a true E2E path (a real ``AIAgent`` flush
+against a real ``SessionDB`` in a temp ``HERMES_HOME``, read back through the
+real ``SessionStore.load_transcript``).
+"""
+
+from __future__ import annotations
+
+import sys
+import types
+from unittest.mock import MagicMock
+
+import pytest
+
+
+@pytest.fixture(autouse=True)
+def _mock_dotenv(monkeypatch):
+    """gateway.run imports dotenv at module load; stub so tests run bare."""
+    fake = types.ModuleType("dotenv")
+    fake.load_dotenv = lambda *a, **kw: None
+    monkeypatch.setitem(sys.modules, "dotenv", fake)
+
+
+def _make_runner():
+    from gateway.run import GatewayRunner
+
+    runner = object.__new__(GatewayRunner)
+    return runner
+
+
+# ─────────────────────────────────────────────────────────────────────────
+# Unit: _finalize_shutdown_agents calls the flush hook with the in-flight
+# transcript before teardown.
+# ─────────────────────────────────────────────────────────────────────────
+class _FakeAgent:
+    def __init__(self, session_messages=None, has_flush=True):
+        if session_messages is not None:
+            self._session_messages = session_messages
+        if has_flush:
+            self._flush_messages_to_session_db = MagicMock()
+            self._drop_trailing_empty_response_scaffolding = MagicMock()
+        self.shutdown_memory_provider = MagicMock()
+        self.close = MagicMock()
+        self.session_id = "sess-1"
+
+
+class TestFinalizeShutdownFlushesInflightTranscript:
+    def test_inflight_messages_flushed_before_teardown(self):
+        """The mid-turn transcript (tail = pending tool result) is flushed
+        to the session DB during shutdown finalization."""
+        runner = _make_runner()
+        inflight = [
+            {"role": "user", "content": "scan the repo and summarise"},
+            {"role": "assistant", "content": "", "tool_calls": [
+                {"id": "c1", "function": {"name": "terminal", "arguments": "{}"}}
+            ]},
+            {"role": "tool", "tool_call_id": "c1", "content": "huge output..."},
+        ]
+        agent = _FakeAgent(session_messages=inflight)
+
+        runner._finalize_shutdown_agents({"agent:main:discord:dm:42": agent})
+
+        agent._flush_messages_to_session_db.assert_called_once_with(inflight)
+        # Cleanup still happens after the flush.
+        agent.close.assert_called_once()
+
+    def test_empty_session_messages_not_flushed(self):
+        """An agent that ran no turns (empty list) triggers no flush — there
+        is nothing in flight to persist."""
+        runner = _make_runner()
+        agent = _FakeAgent(session_messages=[])
+
+        runner._finalize_shutdown_agents({"k": agent})
+
+        agent._flush_messages_to_session_db.assert_not_called()
+        agent.close.assert_called_once()
+
+    def test_missing_flush_method_is_tolerated(self):
+        """A stub agent without the flush method (object.__new__ test stubs)
+        must not break shutdown — teardown still runs."""
+        runner = _make_runner()
+        agent = _FakeAgent(session_messages=[{"role": "user", "content": "x"}],
+                           has_flush=False)
+
+        runner._finalize_shutdown_agents({"k": agent})
+
+        agent.close.assert_called_once()
+
+    def test_flush_exception_is_swallowed(self):
+        """A raising flush must not prevent teardown — a transcript-flush
+        failure is best-effort, losing tool resources is worse."""
+        runner = _make_runner()
+        agent = _FakeAgent(session_messages=[{"role": "user", "content": "x"}])
+        agent._flush_messages_to_session_db.side_effect = RuntimeError("db locked")
+
+        runner._finalize_shutdown_agents({"k": agent})
+
+        agent.close.assert_called_once()
+
+
+# ─────────────────────────────────────────────────────────────────────────
+# E2E: real AIAgent flush → real SessionDB → real load_transcript.
+# ─────────────────────────────────────────────────────────────────────────
+class TestShutdownTranscriptSurvivesResumeE2E:
+    def test_interrupted_turn_persisted_and_readable_on_resume(self, tmp_path, monkeypatch):
+        """Drive the real flush path against a real SessionDB and confirm the
+        in-flight turn is readable back through SessionStore.load_transcript —
+        the exact path the resume logic reads on the next message."""
+        # Isolated state.db.
+        monkeypatch.setenv("HERMES_HOME", str(tmp_path / ".hermes"))
+
+        from hermes_state import SessionDB
+        from run_agent import AIAgent
+
+        db = SessionDB(db_path=tmp_path / "state.db")
+        session_id = "sess-e2e-13121"
+        db.create_session(session_id=session_id, source="discord")
+
+        # Simulate a session whose FIRST turn completed and was persisted...
+        db.append_message(session_id=session_id, role="user",
+                          content="hello, remember my cat is Mochi")
+        db.append_message(session_id=session_id, role="assistant",
+                          content="Noted — Mochi the cat.")
+
+        # ...and a SECOND turn that was interrupted mid tool-loop. These rows
+        # were NEVER flushed to the DB (only live in _session_messages).
+        prior_history = [
+            {"role": "user", "content": "hello, remember my cat is Mochi"},
+            {"role": "assistant", "content": "Noted — Mochi the cat."},
+        ]
+        inflight_tail = [
+            {"role": "user", "content": "now scan the whole repo for TODOs"},
+            {"role": "assistant", "content": "", "tool_calls": [
+                {"id": "tc1", "function": {"name": "terminal",
+                                           "arguments": "{\"command\": \"grep -r TODO\"}"}}
+            ]},
+            {"role": "tool", "tool_call_id": "tc1", "name": "terminal",
+             "content": "src/a.py: TODO fix this\nsrc/b.py: TODO and that"},
+        ]
+        # _session_messages is the live list: history copy + in-flight tail.
+        session_messages = list(prior_history) + list(inflight_tail)
+
+        # Build a real AIAgent shaped only with what the flush path reads.
+        agent = object.__new__(AIAgent)
+        agent._session_db = db
+        agent._session_db_created = True
+        agent.session_id = session_id
+        agent.platform = "discord"
+        agent._session_messages = session_messages
+        # Model a real agent: turn 1 already flushed, so its message identities
+        # are recorded in the dedup set. Only the in-flight turn-2 tail is new.
+        agent._last_flushed_db_idx = len(prior_history)
+        agent._flushed_db_message_ids = {id(m) for m in prior_history}
+        agent._flushed_db_message_session_id = session_id
+
+        # Sanity: only the 2 first-turn rows are in the DB before shutdown.
+        before = db.get_messages_as_conversation(session_id)
+        assert len(before) == 2, before
+
+        # Drive the gateway shutdown finalization with this real agent.
+        from gateway.run import GatewayRunner
+        runner = object.__new__(GatewayRunner)
+        runner._finalize_shutdown_agents({"agent:main:discord:dm:7": agent})
+
+        # The in-flight turn must now be durable and readable via the SAME
+        # path the resume logic uses (SessionStore.load_transcript → DB).
+        after = db.get_messages_as_conversation(session_id)
+        roles = [m.get("role") for m in after]
+        contents = [m.get("content") for m in after]
+
+        assert len(after) == 5, after
+        # The interrupted user message survived.
+        assert any("scan the whole repo for TODOs" in (c or "") for c in contents), contents
+        # The pending tool result (the immediate pre-restart context) survived.
+        assert any("TODO fix this" in (c or "") for c in contents), contents
+        # Tail is a tool result — exactly what the _has_fresh_tool_tail resume
+        # branch in _handle_message_with_agent expects to handle.
+        assert roles[-1] == "tool", roles
+
+    def test_graceful_agent_reflush_is_idempotent(self, tmp_path, monkeypatch):
+        """An agent that already flushed via finalize_turn must not produce
+        duplicate rows when _finalize_shutdown_agents re-flushes."""
+        monkeypatch.setenv("HERMES_HOME", str(tmp_path / ".hermes"))
+
+        from hermes_state import SessionDB
+        from run_agent import AIAgent
+
+        db = SessionDB(db_path=tmp_path / "state.db")
+        session_id = "sess-e2e-idem"
+        db.create_session(session_id=session_id, source="discord")
+
+        msgs = [
+            {"role": "user", "content": "what is 2+2"},
+            {"role": "assistant", "content": "4"},
+        ]
+
+        agent = object.__new__(AIAgent)
+        agent._session_db = db
+        agent._session_db_created = True
+        agent.session_id = session_id
+        agent.platform = "discord"
+        agent._session_messages = msgs
+        agent._last_flushed_db_idx = 0
+        agent._flushed_db_message_ids = set()
+        agent._flushed_db_message_session_id = None
+
+        # First flush (simulating finalize_turn).
+        agent._flush_messages_to_session_db(msgs)
+        assert len(db.get_messages_as_conversation(session_id)) == 2
+
+        # Shutdown re-flush of the SAME list identity must add nothing.
+        from gateway.run import GatewayRunner
+        runner = object.__new__(GatewayRunner)
+        runner._finalize_shutdown_agents({"k": agent})
+
+        after = db.get_messages_as_conversation(session_id)
+        assert len(after) == 2, after