diff --git a/run_agent.py b/run_agent.py
index 4aa3b8332ef1..166ce7dfb97e 100644
--- a/run_agent.py
+++ b/run_agent.py
@@ -1762,8 +1762,23 @@ class AIAgent:
                 # blocks. A list override, however, is the original clean
                 # multimodal payload (for example before a queued /model note)
                 # and must replace the API-local list once the turn is final.
-                if override is not None and (
-                    not isinstance(msg.get("content"), list) or isinstance(override, list)
+                # Preflight compaction can re-anchor this index at a message
+                # whose content was MERGED with the compaction summary
+                # (merge-summary-into-tail).  That is not an accident:
+                # ``reanchor_current_turn_user_idx`` falls back to the last
+                # user row precisely BECAUSE the merge rewrote the content and
+                # the exact-match lookup misses.  Overwriting it with the clean
+                # text would drop the summary from the continuation history the
+                # next turn is built from — the same hazard the DB-write twin
+                # below already refuses (see the sibling guard in
+                # ``_flush_messages_to_session_db_unlocked``).
+                if (
+                    override is not None
+                    and not msg.get(COMPRESSED_SUMMARY_METADATA_KEY)
+                    and (
+                        not isinstance(msg.get("content"), list)
+                        or isinstance(override, list)
+                    )
                 ):
                     msg["content"] = override
                 if timestamp is not None:
diff --git a/tests/agent/test_api_content_sidecar.py b/tests/agent/test_api_content_sidecar.py
index b78fab9f84f2..68bc6bf15e2f 100644
--- a/tests/agent/test_api_content_sidecar.py
+++ b/tests/agent/test_api_content_sidecar.py
@@ -776,6 +776,67 @@ class TestFlushCompressedSummaryOverrideGuard:
         finally:
             db.close()
 
+    def test_live_override_skipped_for_compression_merged_row(self, tmp_path):
+        """Same invariant as the test above, for the in-memory path.
+
+        ``finalize_turn`` calls ``_apply_persist_user_message_override`` and
+        only then ``_persist_session``, so the live dict is rewritten BEFORE
+        the DB-write guard above ever sees it. A compaction-merged row must
+        survive: the summary is the whole pre-compaction history, and this
+        list is the continuation history the next turn is built from.
+        """
+        from agent.context_compressor import COMPRESSED_SUMMARY_METADATA_KEY
+
+        db = SessionDB(db_path=tmp_path / "state.db")
+        sid = "sess-merged-live"
+        db.create_session(session_id=sid, source="cli")
+        try:
+            agent = self._make_agent(db, sid)
+            merged = "[prior context]\ncompaction summary\n\nactual question"
+            messages = [
+                {
+                    "role": "user",
+                    "content": merged,
+                    COMPRESSED_SUMMARY_METADATA_KEY: True,
+                }
+            ]
+            agent._persist_user_message_idx = 0
+            agent._persist_user_message_override = "actual question"
+            agent._persist_user_message_timestamp = 1730000000
+
+            agent._apply_persist_user_message_override(messages)
+
+            assert messages[0]["content"] == merged, (
+                "the compaction summary was erased from the continuation history"
+            )
+            # The paired timestamp override is unrelated and still applies.
+            assert messages[0]["timestamp"] == 1730000000
+        finally:
+            db.close()
+
+    def test_live_override_still_applies_without_merge_marker(self, tmp_path):
+        """Negative control: an ordinary turn is still cleaned in place."""
+        db = SessionDB(db_path=tmp_path / "state.db")
+        sid = "sess-plain-live"
+        db.create_session(session_id=sid, source="cli")
+        try:
+            agent = self._make_agent(db, sid)
+            messages = [
+                {
+                    "role": "user",
+                    "content": "[gateway note] observed\n\nactual question",
+                }
+            ]
+            agent._persist_user_message_idx = 0
+            agent._persist_user_message_override = "actual question"
+            agent._persist_user_message_timestamp = None
+
+            agent._apply_persist_user_message_override(messages)
+
+            assert messages[0]["content"] == "actual question"
+        finally:
+            db.close()
+
 
 class TestFlushSanitizeDivergenceCapture:
     def _make_agent(self, db, sid):