diff --git a/codex-rs/core/src/agent/control/spawn.rs b/codex-rs/core/src/agent/control/spawn.rs
index 7cf5d00b4..8df3b0a07 100644
--- a/codex-rs/core/src/agent/control/spawn.rs
+++ b/codex-rs/core/src/agent/control/spawn.rs
@@ -109,6 +109,79 @@ impl AgentControl {
             .await
     }
 
+    pub(crate) async fn ensure_v2_agent_loaded(
+        &self,
+        config: Config,
+        thread_id: ThreadId,
+    ) -> CodexResult<()> {
+        let state = self.upgrade()?;
+        if state.get_thread(thread_id).await.is_ok() {
+            return Ok(());
+        }
+        if self.state.agent_metadata_for_thread(thread_id).is_none() {
+            return Err(CodexErr::ThreadNotFound(thread_id));
+        }
+
+        let stored_thread = state
+            .read_stored_thread(ReadThreadParams {
+                thread_id,
+                include_archived: true,
+                include_history: true,
+            })
+            .await?;
+        let stored_source = stored_thread.source.clone();
+        let stored_parent_thread_id = stored_thread.parent_thread_id;
+        let history = stored_thread
+            .history
+            .ok_or(CodexErr::ThreadNotFound(thread_id))?
+            .items;
+        let initial_history = InitialHistory::Resumed(ResumedHistory {
+            conversation_id: thread_id,
+            history,
+            rollout_path: stored_thread.rollout_path,
+        });
+        if initial_history.get_multi_agent_version() != Some(MultiAgentVersion::V2) {
+            return Err(CodexErr::ThreadNotFound(thread_id));
+        }
+
+        let (session_source, _) = initial_history
+            .get_resumed_session_sources()
+            .unwrap_or((stored_source, None));
+        let parent_thread_id = initial_history
+            .get_resumed_parent_thread_id()
+            .or(stored_parent_thread_id);
+        let inherited_shell_snapshot = self
+            .inherited_shell_snapshot_for_source(&state, Some(&session_source))
+            .await;
+        let inherited_exec_policy = self
+            .inherited_exec_policy_for_source(&state, Some(&session_source), &config)
+            .await;
+
+        match state
+            .resume_thread_with_history_with_source(ResumeThreadWithHistoryOptions {
+                config,
+                initial_history,
+                agent_control: self.clone(),
+                session_source,
+                parent_thread_id,
+                inherited_shell_snapshot,
+                inherited_exec_policy,
+            })
+            .await
+        {
+            Ok(reloaded_thread) => {
+                state.notify_thread_created(reloaded_thread.thread_id);
+                Ok(())
+            }
+            Err(err) => {
+                if state.get_thread(thread_id).await.is_ok() {
+                    return Ok(());
+                }
+                Err(err)
+            }
+        }
+    }
+
     async fn spawn_agent_internal(
         &self,
         config: Config,
diff --git a/codex-rs/core/src/agent/control_tests.rs b/codex-rs/core/src/agent/control_tests.rs
index 3866d2201..c9cd44492 100644
--- a/codex-rs/core/src/agent/control_tests.rs
+++ b/codex-rs/core/src/agent/control_tests.rs
@@ -527,6 +527,113 @@ async fn send_inter_agent_communication_without_turn_queues_message_without_trig
     ));
 }
 
+#[tokio::test]
+async fn ensure_v2_agent_loaded_reloads_registered_unloaded_agent() {
+    let (home, mut config) = test_config().await;
+    let _ = config.features.enable(Feature::MultiAgentV2);
+    let _ = config.features.enable(Feature::Sqlite);
+    let state_db = init_state_db(&config).await;
+    let manager = ThreadManager::with_models_provider_home_and_state_for_tests(
+        CodexAuth::from_api_key("dummy"),
+        config.model_provider.clone(),
+        config.codex_home.to_path_buf(),
+        std::sync::Arc::new(codex_exec_server::EnvironmentManager::default_for_tests()),
+        state_db.clone(),
+    );
+    let control = manager.agent_control();
+    let harness = AgentControlHarness {
+        _home: home,
+        config,
+        state_db,
+        manager,
+        control,
+    };
+    let (parent_thread_id, _parent_thread) = harness.start_thread().await;
+    let agent_path = AgentPath::try_from("/root/worker").expect("agent path");
+    let spawned_agent = harness
+        .control
+        .spawn_agent_with_metadata(
+            harness.config.clone(),
+            text_input("hello child"),
+            Some(SessionSource::SubAgent(SubAgentSource::ThreadSpawn {
+                parent_thread_id,
+                depth: 1,
+                agent_path: Some(agent_path.clone()),
+                agent_nickname: None,
+                agent_role: None,
+            })),
+            SpawnAgentOptions {
+                parent_thread_id: Some(parent_thread_id),
+                ..Default::default()
+            },
+        )
+        .await
+        .expect("spawn_agent should succeed");
+    let child_thread = harness
+        .manager
+        .get_thread(spawned_agent.thread_id)
+        .await
+        .expect("child thread should exist");
+    child_thread
+        .inject_response_items(vec![assistant_message(
+            "child persisted",
+            Some(MessagePhase::FinalAnswer),
+        )])
+        .await
+        .expect("child rollout should persist with v2 metadata");
+    child_thread
+        .shutdown_and_wait()
+        .await
+        .expect("child thread should shut down");
+
+    assert!(
+        harness
+            .manager
+            .remove_thread(&spawned_agent.thread_id)
+            .await
+            .is_some()
+    );
+    match harness.manager.get_thread(spawned_agent.thread_id).await {
+        Err(CodexErr::ThreadNotFound(id)) => assert_eq!(id, spawned_agent.thread_id),
+        Err(err) => panic!("expected ThreadNotFound, got {err:?}"),
+        Ok(_) => panic!("expected thread to be removed"),
+    }
+
+    harness
+        .control
+        .ensure_v2_agent_loaded(harness.config.clone(), spawned_agent.thread_id)
+        .await
+        .expect("known v2 agent should reload");
+    let _ = harness
+        .manager
+        .get_thread(spawned_agent.thread_id)
+        .await
+        .expect("reloaded child thread should exist");
+
+    let communication = InterAgentCommunication::new(
+        AgentPath::root(),
+        agent_path,
+        Vec::new(),
+        "hello after reload".to_string(),
+        /*trigger_turn*/ false,
+    );
+    harness
+        .control
+        .send_inter_agent_communication(spawned_agent.thread_id, communication.clone())
+        .await
+        .expect("send_inter_agent_communication should succeed after reload");
+    let expected = (
+        spawned_agent.thread_id,
+        Op::InterAgentCommunication { communication },
+    );
+    let captured = harness
+        .manager
+        .captured_ops()
+        .into_iter()
+        .find(|entry| *entry == expected);
+    assert_eq!(captured, Some(expected));
+}
+
 #[tokio::test]
 async fn encrypted_inter_agent_communication_clears_existing_last_task_message() {
     let harness = AgentControlHarness::new().await;
diff --git a/codex-rs/core/src/tools/handlers/multi_agents/send_input.rs b/codex-rs/core/src/tools/handlers/multi_agents/send_input.rs
index 1b7018939..6e28d0a1d 100644
--- a/codex-rs/core/src/tools/handlers/multi_agents/send_input.rs
+++ b/codex-rs/core/src/tools/handlers/multi_agents/send_input.rs
@@ -42,8 +42,17 @@ impl ToolExecutor<ToolInvocation> for Handler {
         let receiver_agent = session
             .services
             .agent_control
-            .get_agent_metadata(receiver_thread_id)
-            .unwrap_or_default();
+            .get_agent_metadata(receiver_thread_id);
+        if receiver_agent.is_some() {
+            let resume_config = build_agent_resume_config(turn.as_ref())?;
+            session
+                .services
+                .agent_control
+                .ensure_v2_agent_loaded(resume_config, receiver_thread_id)
+                .await
+                .map_err(|err| collab_agent_error(receiver_thread_id, err))?;
+        }
+        let receiver_agent = receiver_agent.unwrap_or_default();
         if args.interrupt {
             session
                 .services
diff --git a/codex-rs/core/src/tools/handlers/multi_agents_v2/message_tool.rs b/codex-rs/core/src/tools/handlers/multi_agents_v2/message_tool.rs
index f23d700e9..528fa5526 100644
--- a/codex-rs/core/src/tools/handlers/multi_agents_v2/message_tool.rs
+++ b/codex-rs/core/src/tools/handlers/multi_agents_v2/message_tool.rs
@@ -75,7 +75,11 @@ pub(crate) async fn handle_message_string_tool(
         .services
         .agent_control
         .get_agent_metadata(receiver_thread_id)
-        .unwrap_or_default();
+        .ok_or_else(|| {
+            FunctionCallError::RespondToModel(format!(
+                "agent with id {receiver_thread_id} not found"
+            ))
+        })?;
     if mode == MessageDeliveryMode::TriggerTurn
         && receiver_agent
             .agent_path
@@ -86,6 +90,16 @@ pub(crate) async fn handle_message_string_tool(
             "Follow-up tasks can't target the root agent".to_string(),
         ));
     }
+    let receiver_agent_path = receiver_agent.agent_path.clone().ok_or_else(|| {
+        FunctionCallError::RespondToModel("target agent is missing an agent_path".to_string())
+    })?;
+    let resume_config = build_agent_resume_config(turn.as_ref())?;
+    session
+        .services
+        .agent_control
+        .ensure_v2_agent_loaded(resume_config, receiver_thread_id)
+        .await
+        .map_err(|err| collab_agent_error(receiver_thread_id, err))?;
     session
         .send_event(
             &turn,
@@ -99,9 +113,6 @@ pub(crate) async fn handle_message_string_tool(
             .into(),
         )
         .await;
-    let receiver_agent_path = receiver_agent.agent_path.clone().ok_or_else(|| {
-        FunctionCallError::RespondToModel("target agent is missing an agent_path".to_string())
-    })?;
     let author = turn
         .session_source
         .get_agent_path()