diff --git a/tests/tui_gateway/test_prompt_submit_durable_refresh.py b/tests/tui_gateway/test_prompt_submit_durable_refresh.py
new file mode 100644
index 0000000000000..d903bc0fcc109
--- /dev/null
+++ b/tests/tui_gateway/test_prompt_submit_durable_refresh.py
@@ -0,0 +1,140 @@
+from __future__ import annotations
+
+import contextlib
+import logging
+import threading
+
+from tui_gateway.prompt_history_sync import (
+    refresh_resumed_history_before_submit,
+    wrap_prompt_submit,
+)
+
+
+class _FakeDB:
+    def __init__(self, history, *, on_read=None):
+        self.history = list(history)
+        self.on_read = on_read
+        self.reads = 0
+
+    def get_resume_conversations(self, session_key):
+        assert session_key == "cron_session"
+        self.reads += 1
+        if self.on_read is not None:
+            self.on_read()
+        return list(self.history), list(self.history)
+
+
+class _FakeServer:
+    def __init__(self, session, db):
+        self._sessions = {"live-sid": session}
+        self._db = db
+        self.logger = logging.getLogger("test_prompt_submit_durable_refresh")
+
+    def _session_db(self, _session):
+        return contextlib.nullcontext(self._db)
+
+    @staticmethod
+    def sanitize_replay_history(history):
+        return list(history)
+
+
+def _messages(count):
+    return [
+        {"role": "user" if i % 2 == 0 else "assistant", "content": f"m{i}"}
+        for i in range(count)
+    ]
+
+
+def _resumed_session(history):
+    ready = threading.Event()
+    ready.set()
+    return {
+        "history": list(history),
+        "history_lock": threading.Lock(),
+        "history_version": 0,
+        "resume_history_ready": ready,
+        "resume_session_id": "cron_session",
+        "running": False,
+        "session_key": "cron_session",
+    }
+
+
+def test_wrap_refreshes_open_time_prefix_before_prompt_handler_runs():
+    """Regression for #91508: the handler must see all externally persisted rows."""
+    opened_at = _messages(12)
+    durable_after_cron_finished = _messages(37)
+    session = _resumed_session(opened_at)
+    db = _FakeDB(durable_after_cron_finished)
+    server = _FakeServer(session, db)
+    seen = {}
+
+    def handler(_rid, _params):
+        seen["history"] = list(session["history"])
+        return {"ok": True}
+
+    result = wrap_prompt_submit(server, handler)(
+        "1", {"session_id": "live-sid", "text": "follow-up"}
+    )
+
+    assert result == {"ok": True}
+    assert len(seen["history"]) == 37
+    assert seen["history"][-1]["content"] == "m36"
+    assert session["history_version"] == 1
+    assert db.reads == 1
+
+
+def test_refresh_does_not_touch_new_non_resumed_sessions():
+    session = _resumed_session(_messages(2))
+    session.pop("resume_session_id")
+    db = _FakeDB(_messages(8))
+    server = _FakeServer(session, db)
+
+    assert refresh_resumed_history_before_submit(
+        server, {"session_id": "live-sid", "text": "hello"}
+    ) is False
+    assert len(session["history"]) == 2
+    assert session["history_version"] == 0
+    assert db.reads == 0
+
+
+def test_refresh_never_replaces_memory_with_a_shorter_durable_projection():
+    session = _resumed_session(_messages(8))
+    db = _FakeDB(_messages(6))
+    server = _FakeServer(session, db)
+
+    assert refresh_resumed_history_before_submit(
+        server, {"session_id": "live-sid", "text": "hello"}
+    ) is False
+    assert len(session["history"]) == 8
+    assert session["history_version"] == 0
+
+
+def test_local_history_mutation_wins_if_it_races_the_durable_read():
+    session = _resumed_session(_messages(12))
+
+    def mutate_locally():
+        with session["history_lock"]:
+            session["history"] = _messages(13)
+            session["history_version"] += 1
+
+    db = _FakeDB(_messages(37), on_read=mutate_locally)
+    server = _FakeServer(session, db)
+
+    assert refresh_resumed_history_before_submit(
+        server, {"session_id": "live-sid", "text": "hello"}
+    ) is False
+    assert len(session["history"]) == 13
+    assert session["history_version"] == 1
+
+
+def test_busy_session_keeps_the_active_turn_as_history_owner():
+    session = _resumed_session(_messages(12))
+    session["running"] = True
+    db = _FakeDB(_messages(37))
+    server = _FakeServer(session, db)
+
+    assert refresh_resumed_history_before_submit(
+        server, {"session_id": "live-sid", "text": "queued follow-up"}
+    ) is False
+    assert len(session["history"]) == 12
+    assert db.reads == 0
diff --git a/tui_gateway/method_ctx.py b/tui_gateway/method_ctx.py
index a72f802bfaec8..7b5f17a3bc8bc 100644
--- a/tui_gateway/method_ctx.py
+++ b/tui_gateway/method_ctx.py
@@ -48,6 +48,16 @@ def install(self, server) -> None:
             real.__kwdefaults__ = fn.__kwdefaults__
             real.__doc__ = fn.__doc__
             real.__dict__.update(fn.__dict__)
+            if name == "prompt.submit":
+                # A resumed session's model-history snapshot can be advanced by
+                # an external writer (notably cron) without touching this
+                # gateway process. Refresh at the dispatch boundary so the
+                # handler claims the turn only after adopting newer durable
+                # context. Kept here to preserve methods_prompt.py's mechanical
+                # handler split and avoid a second copy of its large body.
+                from .prompt_history_sync import wrap_prompt_submit
+
+                real = wrap_prompt_submit(server, real)
             if getattr(fn, "_hermes_profile_scoped", False):
                 real = server._profile_scoped(real)
             server._methods[name] = real
diff --git a/tui_gateway/prompt_history_sync.py b/tui_gateway/prompt_history_sync.py
new file mode 100644
index 0000000000000..6e01cb8e08dd9
--- /dev/null
+++ b/tui_gateway/prompt_history_sync.py
@@ -0,0 +1,160 @@
+"""Durable-history refresh for resumed ``prompt.submit`` calls.
+
+A resumed Desktop/TUI session keeps an in-memory model-history snapshot. Other
+processes can continue writing the same durable session (cron is the important
+case), so the display transcript may advance while the model snapshot stays at
+its open-time prefix. Before a new turn is claimed, refresh an idle resumed
+session from its owning state.db when the durable model projection has grown.
+"""
+
+from __future__ import annotations
+
+import functools
+import logging
+from typing import Any, Callable
+
+
+_LOG = logging.getLogger(__name__)
+
+
+def _server_logger(server):
+    return getattr(server, "logger", _LOG)
+
+
+def refresh_resumed_history_before_submit(server, params: dict[str, Any]) -> bool:
+    """Adopt newer durable model history for an idle resumed session.
+
+    Returns ``True`` only when ``session['history']`` was replaced. The update
+    is deliberately monotonic: a shorter/equal durable projection never
+    replaces memory, and a local history mutation that races the DB read wins.
+    This keeps the guard safe for queued/live turns while repairing the stale
+    open-time snapshot produced by cross-process writers.
+    """
+    if not isinstance(params, dict):
+        return False
+
+    sid = str(params.get("session_id") or "")
+    sessions = getattr(server, "_sessions", None)
+    session = sessions.get(sid) if isinstance(sessions, dict) else None
+    if not isinstance(session, dict) or not session.get("resume_session_id"):
+        return False
+
+    # Deferred Desktop resumes hydrate once in a background worker. Never race
+    # that assignment: wait for its completion/error signal before taking a
+    # fresh durable snapshot. A bounded wait avoids making prompt dispatch
+    # permanently dependent on a stuck hydration worker.
+    ready = session.get("resume_history_ready")
+    if ready is not None and callable(getattr(ready, "wait", None)):
+        try:
+            if not ready.wait(timeout=30.0):
+                _server_logger(server).warning(
+                    "prompt.submit: resume history still hydrating for session %s; "
+                    "skipping durable refresh",
+                    sid,
+                )
+                return False
+        except Exception:
+            _server_logger(server).debug(
+                "prompt.submit: failed waiting for resume history for session %s",
+                sid,
+                exc_info=True,
+            )
+            return False
+
+    if session.get("resume_history_error"):
+        return False
+
+    lock = session.get("history_lock")
+    if lock is None:
+        return False
+
+    with lock:
+        # A busy submit is handled by the normal queue/interrupt path. Its
+        # active turn owns the in-memory transcript and must not be overwritten
+        # from a concurrent durable read.
+        if session.get("running"):
+            return False
+        start_version = int(session.get("history_version", 0))
+        start_history = list(session.get("history") or [])
+
+    session_key = str(
+        session.get("session_key") or session.get("resume_session_id") or sid
+    )
+    if not session_key:
+        return False
+
+    try:
+        session_db = getattr(server, "_session_db")
+        with session_db(session) as db:
+            if db is None:
+                return False
+            get_resume = getattr(db, "get_resume_conversations", None)
+            if callable(get_resume):
+                raw_history, _display_history = get_resume(session_key)
+            else:
+                get_history = getattr(db, "get_messages_as_conversation", None)
+                if not callable(get_history):
+                    return False
+                raw_history = get_history(
+                    session_key,
+                    repair_alternation=True,
+                    include_row_ids=True,
+                )
+    except Exception:
+        _server_logger(server).debug(
+            "prompt.submit: failed refreshing durable history for resumed session %s",
+            session_key,
+            exc_info=True,
+        )
+        return False
+
+    if not isinstance(raw_history, list):
+        return False
+    sanitize = getattr(server, "sanitize_replay_history", None)
+    try:
+        durable_history = sanitize(raw_history) if callable(sanitize) else raw_history
+    except Exception:
+        _server_logger(server).debug(
+            "prompt.submit: failed sanitizing refreshed history for session %s",
+            session_key,
+            exc_info=True,
+        )
+        return False
+    if not isinstance(durable_history, list):
+        return False
+
+    with lock:
+        # A local mutation after the snapshot wins. Checking both the explicit
+        # version and the value catches legacy/in-place mutations that forgot to
+        # bump history_version.
+        if session.get("running"):
+            return False
+        if int(session.get("history_version", 0)) != start_version:
+            return False
+        if list(session.get("history") or []) != start_history:
+            return False
+        if len(durable_history) <= len(start_history):
+            return False
+
+        session["history"] = list(durable_history)
+        session["history_version"] = start_version + 1
+
+    _server_logger(server).info(
+        "prompt.submit: refreshed resumed session %s history %d -> %d messages "
+        "from durable state",
+        session_key,
+        len(start_history),
+        len(durable_history),
+    )
+    return True
+
+
+def wrap_prompt_submit(server, handler: Callable) -> Callable:
+    """Wrap the registered ``prompt.submit`` handler with the refresh guard."""
+
+    @functools.wraps(handler)
+    def wrapped(rid, params):
+        refresh_resumed_history_before_submit(server, params)
+        return handler(rid, params)
+
+    return wrapped