diff --git a/codex-rs/app-server/src/codex_message_processor.rs b/codex-rs/app-server/src/codex_message_processor.rs
index 6475531c0..86c2218bc 100644
--- a/codex-rs/app-server/src/codex_message_processor.rs
+++ b/codex-rs/app-server/src/codex_message_processor.rs
@@ -2754,6 +2754,24 @@ impl CodexMessageProcessor {
         if state_db_ctx.is_none() {
             state_db_ctx = get_state_db(&self.config).await;
         }
+        if state_db_ctx.is_none() {
+            match StateRuntime::init(
+                self.config.sqlite_home.clone(),
+                self.config.model_provider_id.clone(),
+            )
+            .await
+            {
+                Ok(ctx) => {
+                    state_db_ctx = Some(ctx);
+                }
+                Err(err) => {
+                    warn!(
+                        "failed to initialize state db for thread metadata update at {}: {err}",
+                        self.config.sqlite_home.display()
+                    );
+                }
+            }
+        }
         let Some(state_db_ctx) = state_db_ctx else {
             self.send_internal_error(
                 request_id,
diff --git a/codex-rs/app-server/tests/suite/v2/thread_metadata_update.rs b/codex-rs/app-server/tests/suite/v2/thread_metadata_update.rs
index 8bf9a8a9a..f5c793f74 100644
--- a/codex-rs/app-server/tests/suite/v2/thread_metadata_update.rs
+++ b/codex-rs/app-server/tests/suite/v2/thread_metadata_update.rs
@@ -223,6 +223,59 @@ async fn thread_metadata_update_repairs_missing_sqlite_row_for_stored_thread() -
     Ok(())
 }
 
+#[tokio::test]
+async fn thread_metadata_update_repairs_stored_thread_before_backfill_completes() -> Result<()> {
+    let server = create_mock_responses_server_repeating_assistant("Done").await;
+    let codex_home = TempDir::new()?;
+    create_config_toml(codex_home.path(), &server.uri())?;
+    let _state_db =
+        StateRuntime::init(codex_home.path().to_path_buf(), "mock_provider".into()).await?;
+
+    let preview = "Stored thread preview before backfill";
+    let thread_id = create_fake_rollout(
+        codex_home.path(),
+        "2025-01-05T12-30-00",
+        "2025-01-05T12:30:00Z",
+        preview,
+        Some("mock_provider"),
+        /*git_info*/ None,
+    )?;
+
+    let mut mcp = McpProcess::new(codex_home.path()).await?;
+    timeout(DEFAULT_READ_TIMEOUT, mcp.initialize()).await??;
+
+    let update_id = mcp
+        .send_thread_metadata_update_request(ThreadMetadataUpdateParams {
+            thread_id: thread_id.clone(),
+            git_info: Some(ThreadMetadataGitInfoUpdateParams {
+                sha: None,
+                branch: Some(Some("feature/pending-backfill".to_string())),
+                origin_url: None,
+            }),
+        })
+        .await?;
+    let update_resp: JSONRPCResponse = timeout(
+        DEFAULT_READ_TIMEOUT,
+        mcp.read_stream_until_response_message(RequestId::Integer(update_id)),
+    )
+    .await??;
+    let ThreadMetadataUpdateResponse { thread: updated } =
+        to_response::<ThreadMetadataUpdateResponse>(update_resp)?;
+
+    assert_eq!(updated.id, thread_id);
+    assert_eq!(updated.preview, preview);
+    assert_eq!(
+        updated.git_info,
+        Some(GitInfo {
+            sha: None,
+            branch: Some("feature/pending-backfill".to_string()),
+            origin_url: None,
+        })
+    );
+
+    Ok(())
+}
+
 #[tokio::test]
 async fn thread_metadata_update_repairs_loaded_thread_without_resetting_summary() -> Result<()> {
     let server = create_mock_responses_server_repeating_assistant("Done").await;