diff --git a/agent/title_generator.py b/agent/title_generator.py
index f865aa02d022..64f5b03f977f 100644
--- a/agent/title_generator.py
+++ b/agent/title_generator.py
@@ -237,6 +237,13 @@ def _auto_title_session(
         return
 
     try:
+        latest = session_db.get_session_title(session_id)
+        if latest:
+            logger.debug(
+                "Skipping auto-generated session title because a title was set while generation was in flight: %s",
+                latest,
+            )
+            return
         session_db.set_session_title(session_id, title)
         logger.debug("Auto-generated session title: %s", title)
         if title_callback is not None:
diff --git a/tests/agent/test_title_generator.py b/tests/agent/test_title_generator.py
index 50aa01951abe..0dfbdc57f322 100644
--- a/tests/agent/test_title_generator.py
+++ b/tests/agent/test_title_generator.py
@@ -245,6 +245,23 @@ class TestAutoTitleSession:
             auto_title_session(db, "sess-1", "hi", "hello")
             db.set_session_title.assert_called_once_with("sess-1", "New Title")
 
+    def test_does_not_overwrite_title_set_while_generation_was_in_flight(self):
+        db = MagicMock()
+        db.get_session_title.side_effect = [None, "Manual Title"]
+        seen = []
+
+        with patch("agent.title_generator.generate_title", return_value="Auto Title"):
+            auto_title_session(
+                db,
+                "sess-1",
+                "hi",
+                "hello",
+                title_callback=seen.append,
+            )
+
+        db.set_session_title.assert_not_called()
+        assert seen == []
+
     def test_invokes_title_callback_after_setting_title(self):
         db = MagicMock()
         db.get_session_title.return_value = None