diff --git a/hermes_state.py b/hermes_state.py
index d307db7a7..cfb63bd16 100644
--- a/hermes_state.py
+++ b/hermes_state.py
@@ -4615,8 +4615,19 @@ class SessionDB:
         topic, causing tool progress, approvals, and replies to land
         in the wrong place.  Issue #31501.
 
-        Returns the number of rows deleted (0 when the binding was
-        already absent or the topic-mode tables haven't been
+        When this prune removes the chat's *last* remaining binding,
+        the chat's row in ``telegram_dm_topic_mode`` is also flipped to
+        ``enabled = 0`` in the same transaction.  Otherwise the chat
+        would be left in topic mode with zero lanes — and
+        ``gateway.run._recover_telegram_topic_thread_id`` keeps treating
+        the chat as topic-enabled, lobby messages keep hunting for a
+        binding that no longer exists, and a user who disabled topics in
+        the Telegram client (rather than via ``/topic off``) stays stuck
+        until the next send happens to fail. Clearing the flag makes
+        recovery fully stand down once the dead topics are gone.
+
+        Returns the number of binding rows deleted (0 when the binding
+        was already absent or the topic-mode tables haven't been
         migrated yet — both are silent no-ops; we never raise from
         a cleanup hot path).
         """
@@ -4637,6 +4648,29 @@ class SessionDB:
             except sqlite3.OperationalError:
                 # Tables don't exist yet — nothing to prune.
                 deleted["count"] = 0
+                return
+            if not deleted["count"]:
+                return
+            # If that was the chat's last binding, disable topic mode for
+            # the chat so recovery stops steering lobby messages at a now
+            # empty lane set. Same transaction → no read-after-prune race.
+            try:
+                remaining = conn.execute(
+                    """
+                    SELECT 1 FROM telegram_dm_topic_bindings
+                    WHERE chat_id = ? LIMIT 1
+                    """,
+                    (chat_id,),
+                ).fetchone()
+                if remaining is None:
+                    conn.execute(
+                        "UPDATE telegram_dm_topic_mode "
+                        "SET enabled = 0, updated_at = ? WHERE chat_id = ?",
+                        (time.time(), chat_id),
+                    )
+            except sqlite3.OperationalError:
+                # telegram_dm_topic_mode absent — binding prune still stands.
+                pass
 
         self._execute_write(_do)
         return deleted["count"]
diff --git a/tests/gateway/test_telegram_prune_stale_topic_binding_31501.py b/tests/gateway/test_telegram_prune_stale_topic_binding_31501.py
index 349ae8569..d93d65896 100644
--- a/tests/gateway/test_telegram_prune_stale_topic_binding_31501.py
+++ b/tests/gateway/test_telegram_prune_stale_topic_binding_31501.py
@@ -155,6 +155,71 @@ class TestDeleteTelegramTopicBinding:
         db.close()
 
 
+class TestPruneClearsTopicModeWhenLastBindingGone:
+    """Proactive cleanup (#31501 follow-up): pruning the chat's final
+    binding must also flip ``telegram_dm_topic_mode.enabled`` to 0 so
+    recovery fully stands down — covers the user who disabled topics in
+    the Telegram client without ever running ``/topic off``."""
+
+    def test_clears_enabled_when_last_binding_pruned(self, tmp_path):
+        db = SessionDB(db_path=tmp_path / "state.db")
+        db.enable_telegram_topic_mode(
+            chat_id="5595856929", user_id="5595856929",
+        )
+        _seed_binding(db, thread_id="15287")
+        assert db.is_telegram_topic_mode_enabled(
+            chat_id="5595856929", user_id="5595856929",
+        ) is True
+
+        removed = db.delete_telegram_topic_binding(
+            chat_id="5595856929", thread_id="15287",
+        )
+
+        assert removed == 1
+        assert db.is_telegram_topic_mode_enabled(
+            chat_id="5595856929", user_id="5595856929",
+        ) is False
+        db.close()
+
+    def test_keeps_enabled_while_other_bindings_remain(self, tmp_path):
+        # Deleting one of several topics must NOT disable topic mode —
+        # the chat still has healthy lanes that recovery should serve.
+        db = SessionDB(db_path=tmp_path / "state.db")
+        db.enable_telegram_topic_mode(
+            chat_id="5595856929", user_id="5595856929",
+        )
+        _seed_binding(db, thread_id="15287", session_id="sess-stale")
+        _seed_binding(db, thread_id="15418", session_id="sess-fresh")
+
+        db.delete_telegram_topic_binding(
+            chat_id="5595856929", thread_id="15287",
+        )
+
+        assert db.is_telegram_topic_mode_enabled(
+            chat_id="5595856929", user_id="5595856929",
+        ) is True
+        db.close()
+
+    def test_noop_prune_leaves_enabled_untouched(self, tmp_path):
+        # A prune that matches no row must not flip the flag — there's
+        # still a live binding the (wrong) thread_id didn't match.
+        db = SessionDB(db_path=tmp_path / "state.db")
+        db.enable_telegram_topic_mode(
+            chat_id="5595856929", user_id="5595856929",
+        )
+        _seed_binding(db, thread_id="15287")
+
+        removed = db.delete_telegram_topic_binding(
+            chat_id="5595856929", thread_id="99999",
+        )
+
+        assert removed == 0
+        assert db.is_telegram_topic_mode_enabled(
+            chat_id="5595856929", user_id="5595856929",
+        ) is True
+        db.close()
+
+
 # ---------------------------------------------------------------------------
 # Adapter glue — _prune_stale_dm_topic_binding
 # ---------------------------------------------------------------------------