diff --git a/codex-rs/core/src/realtime_conversation.rs b/codex-rs/core/src/realtime_conversation.rs
index 8842c41c9..e614be106 100644
--- a/codex-rs/core/src/realtime_conversation.rs
+++ b/codex-rs/core/src/realtime_conversation.rs
@@ -373,7 +373,15 @@ pub(crate) async fn handle_audio(
 }
 
 fn realtime_text_from_handoff_request(handoff: &RealtimeHandoffRequested) -> Option<String> {
-    (!handoff.input_transcript.is_empty()).then(|| handoff.input_transcript.clone())
+    let messages = handoff
+        .messages
+        .iter()
+        .map(|message| message.text.as_str())
+        .collect::<Vec<_>>()
+        .join("\n");
+    (!messages.is_empty()).then_some(messages).or_else(|| {
+        (!handoff.input_transcript.is_empty()).then(|| handoff.input_transcript.clone())
+    })
 }
 
 fn realtime_api_key(
@@ -579,19 +587,39 @@ mod tests {
     use pretty_assertions::assert_eq;
 
     #[test]
-    fn extracts_text_from_handoff_request_input_transcript() {
+    fn extracts_text_from_handoff_request_messages() {
         let handoff = RealtimeHandoffRequested {
             handoff_id: "handoff_1".to_string(),
             item_id: "item_1".to_string(),
-            input_transcript: "hello".to_string(),
-            messages: vec![RealtimeHandoffMessage {
-                role: "user".to_string(),
-                text: "hello".to_string(),
-            }],
+            input_transcript: "ignored".to_string(),
+            messages: vec![
+                RealtimeHandoffMessage {
+                    role: "user".to_string(),
+                    text: "hello".to_string(),
+                },
+                RealtimeHandoffMessage {
+                    role: "assistant".to_string(),
+                    text: "hi there".to_string(),
+                },
+            ],
         };
         assert_eq!(
             realtime_text_from_handoff_request(&handoff),
-            Some("hello".to_string())
+            Some("hello\nhi there".to_string())
+        );
+    }
+
+    #[test]
+    fn extracts_text_from_handoff_request_input_transcript_if_messages_missing() {
+        let handoff = RealtimeHandoffRequested {
+            handoff_id: "handoff_1".to_string(),
+            item_id: "item_1".to_string(),
+            input_transcript: "ignored".to_string(),
+            messages: vec![],
+        };
+        assert_eq!(
+            realtime_text_from_handoff_request(&handoff),
+            Some("ignored".to_string())
         );
     }
 
diff --git a/codex-rs/core/tests/suite/realtime_conversation.rs b/codex-rs/core/tests/suite/realtime_conversation.rs
index 32500299c..ff4e745dd 100644
--- a/codex-rs/core/tests/suite/realtime_conversation.rs
+++ b/codex-rs/core/tests/suite/realtime_conversation.rs
@@ -918,6 +918,80 @@ async fn inbound_handoff_request_starts_turn() -> Result<()> {
     Ok(())
 }
 
+#[tokio::test(flavor = "multi_thread", worker_threads = 2)]
+async fn inbound_handoff_request_uses_all_messages() -> Result<()> {
+    skip_if_no_network!(Ok(()));
+
+    let api_server = start_mock_server().await;
+    let response_mock = responses::mount_sse_once(
+        &api_server,
+        responses::sse(vec![
+            responses::ev_response_created("resp-1"),
+            responses::ev_assistant_message("msg-1", "ok"),
+            responses::ev_completed("resp-1"),
+        ]),
+    )
+    .await;
+
+    let realtime_server = start_websocket_server(vec![vec![vec![
+        json!({
+            "type": "session.updated",
+            "session": { "id": "sess_inbound_multi", "instructions": "backend prompt" }
+        }),
+        json!({
+            "type": "conversation.handoff.requested",
+            "handoff_id": "handoff_inbound_multi",
+            "item_id": "item_inbound_multi",
+            "input_transcript": "ignored",
+            "messages": [
+                { "role": "assistant", "text": "assistant context" },
+                { "role": "user", "text": "delegated query" },
+                { "role": "assistant", "text": "assist confirm" },
+            ]
+        }),
+    ]]])
+    .await;
+
+    let mut builder = test_codex().with_config({
+        let realtime_base_url = realtime_server.uri().to_string();
+        move |config| {
+            config.experimental_realtime_ws_base_url = Some(realtime_base_url);
+        }
+    });
+    let test = builder.build(&api_server).await?;
+
+    test.codex
+        .submit(Op::RealtimeConversationStart(ConversationStartParams {
+            prompt: "backend prompt".to_string(),
+            session_id: None,
+        }))
+        .await?;
+
+    let _ = wait_for_event_match(&test.codex, |msg| match msg {
+        EventMsg::RealtimeConversationRealtime(RealtimeConversationRealtimeEvent {
+            payload: RealtimeEvent::SessionUpdated { session_id, .. },
+        }) => Some(session_id.clone()),
+        _ => None,
+    })
+    .await;
+
+    wait_for_event(&test.codex, |event| {
+        matches!(event, EventMsg::TurnComplete(_))
+    })
+    .await;
+
+    let request = response_mock.single_request();
+    let user_texts = request.message_input_texts("user");
+    assert!(
+        user_texts
+            .iter()
+            .any(|text| text == "assistant context\ndelegated query\nassist confirm")
+    );
+
+    realtime_server.shutdown().await;
+    Ok(())
+}
+
 #[tokio::test(flavor = "multi_thread", worker_threads = 2)]
 async fn inbound_conversation_item_does_not_start_turn_and_still_forwards_audio() -> Result<()> {
     skip_if_no_network!(Ok(()));