diff --git a/codex-rs/Cargo.lock b/codex-rs/Cargo.lock
index f69322f8ec..bec80224c0 100644
--- a/codex-rs/Cargo.lock
+++ b/codex-rs/Cargo.lock
@@ -1924,7 +1924,6 @@ dependencies = [
  "codex-git-utils",
  "codex-hooks",
  "codex-instructions",
- "codex-keyring-store",
  "codex-login",
  "codex-mcp",
  "codex-model-provider-info",
diff --git a/codex-rs/app-server-protocol/src/protocol/thread_history.rs b/codex-rs/app-server-protocol/src/protocol/thread_history.rs
index d2296c75c5..6c85612bc9 100644
--- a/codex-rs/app-server-protocol/src/protocol/thread_history.rs
+++ b/codex-rs/app-server-protocol/src/protocol/thread_history.rs
@@ -218,7 +218,9 @@ impl ThreadHistoryBuilder {
             RolloutItem::EventMsg(event) => self.handle_event(event),
             RolloutItem::Compacted(payload) => self.handle_compacted(payload),
             RolloutItem::ResponseItem(item) => self.handle_response_item(item),
-            RolloutItem::TurnContext(_) | RolloutItem::SessionMeta(_) => {}
+            RolloutItem::TurnContext(_)
+            | RolloutItem::SessionMeta(_)
+            | RolloutItem::SessionState(_) => {}
         }
     }
 
diff --git a/codex-rs/app-server/tests/suite/v2/client_metadata.rs b/codex-rs/app-server/tests/suite/v2/client_metadata.rs
index c85febd7d4..e343e08470 100644
--- a/codex-rs/app-server/tests/suite/v2/client_metadata.rs
+++ b/codex-rs/app-server/tests/suite/v2/client_metadata.rs
@@ -18,7 +18,7 @@ use std::path::Path;
 use tempfile::TempDir;
 use tokio::time::timeout;
 
-const DEFAULT_READ_TIMEOUT: std::time::Duration = std::time::Duration::from_secs(10);
+const DEFAULT_READ_TIMEOUT: std::time::Duration = std::time::Duration::from_secs(20);
 
 #[tokio::test]
 async fn turn_start_forwards_client_metadata_to_responses_request_v2() -> Result<()> {
diff --git a/codex-rs/app-server/tests/suite/v2/collaboration_mode_list.rs b/codex-rs/app-server/tests/suite/v2/collaboration_mode_list.rs
index 7c36827e6d..0dd4e8174a 100644
--- a/codex-rs/app-server/tests/suite/v2/collaboration_mode_list.rs
+++ b/codex-rs/app-server/tests/suite/v2/collaboration_mode_list.rs
@@ -21,7 +21,7 @@ use pretty_assertions::assert_eq;
 use tempfile::TempDir;
 use tokio::time::timeout;
 
-const DEFAULT_TIMEOUT: Duration = Duration::from_secs(10);
+const DEFAULT_TIMEOUT: Duration = Duration::from_secs(20);
 
 /// Confirms the server returns the default collaboration mode presets in a stable order.
 #[tokio::test]
diff --git a/codex-rs/app-server/tests/suite/v2/connection_handling_websocket.rs b/codex-rs/app-server/tests/suite/v2/connection_handling_websocket.rs
index 30caa13761..e6818eabd7 100644
--- a/codex-rs/app-server/tests/suite/v2/connection_handling_websocket.rs
+++ b/codex-rs/app-server/tests/suite/v2/connection_handling_websocket.rs
@@ -47,7 +47,7 @@ use tokio_tungstenite::tungstenite::http::HeaderValue;
 use tokio_tungstenite::tungstenite::http::header::AUTHORIZATION;
 use tokio_tungstenite::tungstenite::http::header::ORIGIN;
 
-pub(super) const DEFAULT_READ_TIMEOUT: Duration = Duration::from_secs(10);
+pub(super) const DEFAULT_READ_TIMEOUT: Duration = Duration::from_secs(20);
 
 pub(super) type WsClient = WebSocketStream<MaybeTlsStream<tokio::net::TcpStream>>;
 type HmacSha256 = Hmac<Sha256>;
diff --git a/codex-rs/app-server/tests/suite/v2/initialize.rs b/codex-rs/app-server/tests/suite/v2/initialize.rs
index 165160468f..cfb08a1718 100644
--- a/codex-rs/app-server/tests/suite/v2/initialize.rs
+++ b/codex-rs/app-server/tests/suite/v2/initialize.rs
@@ -24,7 +24,7 @@ use std::time::Duration;
 use tempfile::TempDir;
 use tokio::time::timeout;
 
-const DEFAULT_READ_TIMEOUT: std::time::Duration = std::time::Duration::from_secs(10);
+const DEFAULT_READ_TIMEOUT: std::time::Duration = std::time::Duration::from_secs(20);
 
 #[tokio::test]
 async fn initialize_uses_client_info_name_as_originator() -> Result<()> {
diff --git a/codex-rs/app-server/tests/suite/v2/realtime_conversation.rs b/codex-rs/app-server/tests/suite/v2/realtime_conversation.rs
index efc167c9d0..4c1b80498c 100644
--- a/codex-rs/app-server/tests/suite/v2/realtime_conversation.rs
+++ b/codex-rs/app-server/tests/suite/v2/realtime_conversation.rs
@@ -69,7 +69,7 @@ use wiremock::matchers::method;
 use wiremock::matchers::path;
 use wiremock::matchers::path_regex;
 
-const DEFAULT_TIMEOUT: Duration = Duration::from_secs(10);
+const DEFAULT_TIMEOUT: Duration = Duration::from_secs(20);
 const STARTUP_CONTEXT_HEADER: &str = "Startup context from Codex.";
 const V2_STEERING_ACKNOWLEDGEMENT: &str =
     "This was sent to steer the previous background agent task.";
@@ -1574,7 +1574,7 @@ async fn webrtc_v2_tool_call_delegated_turn_can_execute_shell_tool() -> Result<(
         create_shell_command_sse_response(
             realtime_tool_ok_command(),
             /*workdir*/ None,
-            Some(5000),
+            Some(10_000),
             "shell_call",
         )?,
         create_final_assistant_message_sse_response("shell tool finished")?,
diff --git a/codex-rs/core/Cargo.toml b/codex-rs/core/Cargo.toml
index 7b3acd6460..e45bf3d258 100644
--- a/codex-rs/core/Cargo.toml
+++ b/codex-rs/core/Cargo.toml
@@ -147,7 +147,6 @@ codex-shell-escalation = { workspace = true }
 assert_cmd = { workspace = true }
 assert_matches = { workspace = true }
 codex-arg0 = { workspace = true }
-codex-keyring-store = { workspace = true }
 codex-otel = { workspace = true }
 codex-utils-cargo-bin = { workspace = true }
 core_test_support = { workspace = true }
diff --git a/codex-rs/core/src/agent/control.rs b/codex-rs/core/src/agent/control.rs
index 509a578f5c..d7a6403c93 100644
--- a/codex-rs/core/src/agent/control.rs
+++ b/codex-rs/core/src/agent/control.rs
@@ -116,6 +116,7 @@ fn keep_forked_rollout_item(item: &RolloutItem) -> bool {
             | ResponseItem::Compaction { .. }
             | ResponseItem::Other,
         ) => false,
+        RolloutItem::SessionState(_) => false,
         RolloutItem::Compacted(_)
         | RolloutItem::EventMsg(_)
         | RolloutItem::SessionMeta(_)
diff --git a/codex-rs/core/src/agent/control_tests.rs b/codex-rs/core/src/agent/control_tests.rs
index d332853167..e3070c6401 100644
--- a/codex-rs/core/src/agent/control_tests.rs
+++ b/codex-rs/core/src/agent/control_tests.rs
@@ -186,7 +186,7 @@ async fn wait_for_subagent_notification(parent_thread: &Arc<CodexThread>) -> boo
             sleep(Duration::from_millis(25)).await;
         }
     };
-    timeout(Duration::from_secs(2), wait).await.is_ok()
+    timeout(Duration::from_secs(5), wait).await.is_ok()
 }
 
 async fn persist_thread_for_tree_resume(thread: &Arc<CodexThread>, message: &str) {
diff --git a/codex-rs/core/src/agent_identity.rs b/codex-rs/core/src/agent_identity.rs
index d799f15846..71c759e59e 100644
--- a/codex-rs/core/src/agent_identity.rs
+++ b/codex-rs/core/src/agent_identity.rs
@@ -153,14 +153,16 @@ impl AgentIdentityManager {
         Ok(stored_identity)
     }
 
-    pub(crate) async fn task_matches_current_binding(&self, task: &RegisteredAgentTask) -> bool {
+    pub(crate) async fn task_matches_current_identity(&self, task: &RegisteredAgentTask) -> bool {
         if !self.feature_enabled {
             return false;
         }
 
-        self.current_auth_binding()
+        self.current_stored_identity()
             .await
-            .is_some_and(|(_, binding)| task.matches_binding(&binding))
+            .is_some_and(|stored_identity| {
+                stored_identity.agent_runtime_id == task.agent_runtime_id
+            })
     }
 
     async fn current_auth_binding(&self) -> Option<(CodexAuth, AgentIdentityBinding)> {
@@ -177,6 +179,11 @@ impl AgentIdentityManager {
         binding.map(|binding| (auth, binding))
     }
 
+    async fn current_stored_identity(&self) -> Option<StoredAgentIdentity> {
+        let (auth, binding) = self.current_auth_binding().await?;
+        self.load_stored_identity(&auth, &binding).ok().flatten()
+    }
+
     async fn register_agent_identity(
         &self,
         binding: &AgentIdentityBinding,
diff --git a/codex-rs/core/src/agent_identity/task_registration.rs b/codex-rs/core/src/agent_identity/task_registration.rs
index 30d2567f28..9bbc364db3 100644
--- a/codex-rs/core/src/agent_identity/task_registration.rs
+++ b/codex-rs/core/src/agent_identity/task_registration.rs
@@ -2,6 +2,7 @@ use std::time::Duration;
 
 use anyhow::Context;
 use anyhow::Result;
+use codex_protocol::protocol::SessionAgentTask;
 use crypto_box::SecretKey as Curve25519SecretKey;
 use ed25519_dalek::Signer as _;
 use serde::Deserialize;
@@ -16,9 +17,6 @@ const AGENT_TASK_REGISTRATION_TIMEOUT: Duration = Duration::from_secs(15);
 
 #[derive(Clone, Debug, PartialEq, Eq)]
 pub(crate) struct RegisteredAgentTask {
-    pub(crate) binding_id: String,
-    pub(crate) chatgpt_account_id: String,
-    pub(crate) chatgpt_user_id: Option<String>,
     pub(crate) agent_runtime_id: String,
     pub(crate) task_id: String,
     pub(crate) registered_at: String,
@@ -82,9 +80,6 @@ impl AgentIdentityManager {
                 .await
                 .with_context(|| format!("failed to parse agent task response from {url}"))?;
             let registered_task = RegisteredAgentTask {
-                binding_id: stored_identity.binding_id.clone(),
-                chatgpt_account_id: stored_identity.chatgpt_account_id.clone(),
-                chatgpt_user_id: stored_identity.chatgpt_user_id.clone(),
                 agent_runtime_id: stored_identity.agent_runtime_id.clone(),
                 task_id: decrypt_task_id_response(
                     &stored_identity,
@@ -107,18 +102,20 @@ impl AgentIdentityManager {
 }
 
 impl RegisteredAgentTask {
-    pub(super) fn matches_binding(&self, binding: &AgentIdentityBinding) -> bool {
-        binding.matches_parts(
-            &self.binding_id,
-            &self.chatgpt_account_id,
-            self.chatgpt_user_id.as_deref(),
-        )
+    pub(crate) fn to_session_agent_task(&self) -> SessionAgentTask {
+        SessionAgentTask {
+            agent_runtime_id: self.agent_runtime_id.clone(),
+            task_id: self.task_id.clone(),
+            registered_at: self.registered_at.clone(),
+        }
     }
 
-    pub(crate) fn has_same_binding(&self, other: &Self) -> bool {
-        self.binding_id == other.binding_id
-            && self.chatgpt_account_id == other.chatgpt_account_id
-            && self.chatgpt_user_id == other.chatgpt_user_id
+    pub(crate) fn from_session_agent_task(task: SessionAgentTask) -> Self {
+        Self {
+            agent_runtime_id: task.agent_runtime_id,
+            task_id: task.task_id,
+            registered_at: task.registered_at,
+        }
     }
 }
 
@@ -242,9 +239,6 @@ mod tests {
         assert_eq!(
             task,
             RegisteredAgentTask {
-                binding_id: "chatgpt-account-account-123".to_string(),
-                chatgpt_account_id: "account-123".to_string(),
-                chatgpt_user_id: Some("user-123".to_string()),
                 agent_runtime_id: "agent-123".to_string(),
                 task_id: "task_123".to_string(),
                 registered_at: task.registered_at.clone(),
@@ -331,9 +325,6 @@ mod tests {
         assert_eq!(
             task,
             RegisteredAgentTask {
-                binding_id: "chatgpt-account-account-123".to_string(),
-                chatgpt_account_id: "account-123".to_string(),
-                chatgpt_user_id: Some("user-123".to_string()),
                 agent_runtime_id: "agent-123".to_string(),
                 task_id: "task_123".to_string(),
                 registered_at: task.registered_at.clone(),
@@ -342,7 +333,7 @@ mod tests {
     }
 
     #[tokio::test]
-    async fn task_matches_current_binding_rejects_stale_auth_binding() {
+    async fn task_matches_current_identity_rejects_stale_registered_identity() {
         let auth_manager =
             AuthManager::from_auth_for_testing(make_chatgpt_auth("account-456", Some("user-456")));
         let manager = AgentIdentityManager::new_for_tests(
@@ -352,15 +343,12 @@ mod tests {
             SessionSource::Cli,
         );
         let task = RegisteredAgentTask {
-            binding_id: "chatgpt-account-account-123".to_string(),
-            chatgpt_account_id: "account-123".to_string(),
-            chatgpt_user_id: Some("user-123".to_string()),
             agent_runtime_id: "agent-123".to_string(),
             task_id: "task_123".to_string(),
             registered_at: "2026-03-23T12:00:00Z".to_string(),
         };
 
-        assert!(!manager.task_matches_current_binding(&task).await);
+        assert!(!manager.task_matches_current_identity(&task).await);
     }
 
     async fn mount_human_biscuit(
diff --git a/codex-rs/core/src/codex.rs b/codex-rs/core/src/codex.rs
index 6128f27035..a2398849df 100644
--- a/codex-rs/core/src/codex.rs
+++ b/codex-rs/core/src/codex.rs
@@ -121,6 +121,7 @@ use codex_protocol::protocol::RawResponseItemEvent;
 use codex_protocol::protocol::ReviewRequest;
 use codex_protocol::protocol::RolloutItem;
 use codex_protocol::protocol::SessionSource;
+use codex_protocol::protocol::SessionStateUpdate;
 use codex_protocol::protocol::SubAgentSource;
 use codex_protocol::protocol::TurnAbortReason;
 use codex_protocol::protocol::TurnContextItem;
@@ -845,6 +846,7 @@ pub(crate) struct Session {
     pub(crate) services: SessionServices,
     js_repl: Arc<JsReplHandle>,
     next_internal_sub_id: AtomicU64,
+    agent_task_registration_lock: Mutex<()>,
 }
 
 #[derive(Clone, Debug)]
@@ -1529,7 +1531,68 @@ impl Session {
         handlers::shutdown(self, self.next_internal_sub_id()).await;
     }
 
-    async fn cached_agent_task_for_current_binding(&self) -> Option<RegisteredAgentTask> {
+    fn latest_persisted_agent_task(
+        rollout_items: &[RolloutItem],
+    ) -> Option<Option<RegisteredAgentTask>> {
+        rollout_items.iter().rev().find_map(|item| match item {
+            RolloutItem::SessionState(update) => Some(
+                update
+                    .agent_task
+                    .clone()
+                    .map(RegisteredAgentTask::from_session_agent_task),
+            ),
+            _ => None,
+        })
+    }
+
+    async fn restore_persisted_agent_task(&self, rollout_items: &[RolloutItem]) {
+        let Some(agent_task) = Self::latest_persisted_agent_task(rollout_items).flatten() else {
+            return;
+        };
+
+        let mut state = self.state.lock().await;
+        state.set_agent_task(agent_task);
+    }
+
+    async fn persist_agent_task_update(&self, agent_task: Option<&RegisteredAgentTask>) {
+        self.persist_rollout_items(&[RolloutItem::SessionState(SessionStateUpdate {
+            agent_task: agent_task.map(RegisteredAgentTask::to_session_agent_task),
+        })])
+        .await;
+    }
+
+    async fn clear_cached_agent_task(&self, agent_task: &RegisteredAgentTask) {
+        let cleared = {
+            let mut state = self.state.lock().await;
+            if state.agent_task().as_ref() == Some(agent_task) {
+                state.clear_agent_task();
+                true
+            } else {
+                false
+            }
+        };
+        if cleared {
+            self.persist_agent_task_update(/*agent_task*/ None).await;
+        }
+    }
+
+    async fn cache_agent_task(&self, agent_task: RegisteredAgentTask) -> RegisteredAgentTask {
+        let changed = {
+            let mut state = self.state.lock().await;
+            if state.agent_task().as_ref() == Some(&agent_task) {
+                false
+            } else {
+                state.set_agent_task(agent_task.clone());
+                true
+            }
+        };
+        if changed {
+            self.persist_agent_task_update(Some(&agent_task)).await;
+        }
+        agent_task
+    }
+
+    async fn cached_agent_task_for_current_identity(&self) -> Option<RegisteredAgentTask> {
         let agent_task = {
             let state = self.state.lock().await;
             state.agent_task()
@@ -1538,7 +1601,7 @@ impl Session {
         if self
             .services
             .agent_identity_manager
-            .task_matches_current_binding(&agent_task)
+            .task_matches_current_identity(&agent_task)
             .await
         {
             debug!(
@@ -1552,17 +1615,19 @@ impl Session {
         debug!(
             agent_runtime_id = %agent_task.agent_runtime_id,
             task_id = %agent_task.task_id,
-            "discarding cached agent task because auth binding changed"
+            "discarding cached agent task because the registered agent identity changed"
         );
-        let mut state = self.state.lock().await;
-        if state.agent_task().as_ref() == Some(&agent_task) {
-            state.clear_agent_task();
-        }
+        self.clear_cached_agent_task(&agent_task).await;
         None
     }
 
     async fn ensure_agent_task_registered(&self) -> anyhow::Result<Option<RegisteredAgentTask>> {
-        if let Some(agent_task) = self.cached_agent_task_for_current_binding().await {
+        if let Some(agent_task) = self.cached_agent_task_for_current_identity().await {
+            return Ok(Some(agent_task));
+        }
+
+        let _guard = self.agent_task_registration_lock.lock().await;
+        if let Some(agent_task) = self.cached_agent_task_for_current_identity().await {
             return Ok(Some(agent_task));
         }
 
@@ -1575,31 +1640,18 @@ impl Session {
             if !self
                 .services
                 .agent_identity_manager
-                .task_matches_current_binding(&agent_task)
+                .task_matches_current_identity(&agent_task)
                 .await
             {
                 debug!(
                     agent_runtime_id = %agent_task.agent_runtime_id,
                     task_id = %agent_task.task_id,
-                    "discarding newly registered agent task because auth binding changed"
+                    "discarding newly registered agent task because the registered agent identity changed"
                 );
                 continue;
             }
 
-            {
-                let mut state = self.state.lock().await;
-                if let Some(existing_agent_task) = state.agent_task() {
-                    if existing_agent_task.has_same_binding(&agent_task) {
-                        return Ok(Some(existing_agent_task));
-                    }
-                    debug!(
-                        agent_runtime_id = %existing_agent_task.agent_runtime_id,
-                        task_id = %existing_agent_task.task_id,
-                        "replacing cached agent task because auth binding changed"
-                    );
-                }
-                state.set_agent_task(agent_task.clone());
-            }
+            let agent_task = self.cache_agent_task(agent_task).await;
 
             info!(
                 thread_id = %self.conversation_id,
@@ -2221,6 +2273,7 @@ impl Session {
             services,
             js_repl,
             next_internal_sub_id: AtomicU64::new(0),
+            agent_task_registration_lock: Mutex::new(()),
         });
         if let Some(network_policy_decider_session) = network_policy_decider_session {
             let mut guard = network_policy_decider_session.write().await;
@@ -2490,6 +2543,7 @@ impl Session {
             }
             InitialHistory::Resumed(resumed_history) => {
                 let rollout_items = resumed_history.history;
+                self.restore_persisted_agent_task(&rollout_items).await;
                 let previous_turn_settings = self
                     .apply_rollout_reconstruction(&turn_context, &rollout_items)
                     .await;
diff --git a/codex-rs/core/src/codex/rollout_reconstruction.rs b/codex-rs/core/src/codex/rollout_reconstruction.rs
index a4c042af0c..3e407c4cd7 100644
--- a/codex-rs/core/src/codex/rollout_reconstruction.rs
+++ b/codex-rs/core/src/codex/rollout_reconstruction.rs
@@ -207,7 +207,9 @@ impl Session {
                         active_segment.get_or_insert_with(ActiveReplaySegment::default);
                     active_segment.counts_as_user_turn |= is_user_turn_boundary(response_item);
                 }
-                RolloutItem::EventMsg(_) | RolloutItem::SessionMeta(_) => {}
+                RolloutItem::EventMsg(_)
+                | RolloutItem::SessionMeta(_)
+                | RolloutItem::SessionState(_) => {}
             }
 
             if base_replacement_history.is_some()
@@ -275,6 +277,7 @@ impl Session {
                     history.drop_last_n_user_turns(rollback.num_turns);
                 }
                 RolloutItem::EventMsg(_)
+                | RolloutItem::SessionState(_)
                 | RolloutItem::TurnContext(_)
                 | RolloutItem::SessionMeta(_) => {}
             }
diff --git a/codex-rs/core/src/codex_tests.rs b/codex-rs/core/src/codex_tests.rs
index c4c5000749..9e5957b003 100644
--- a/codex-rs/core/src/codex_tests.rs
+++ b/codex-rs/core/src/codex_tests.rs
@@ -1077,6 +1077,67 @@ async fn record_initial_history_reconstructs_resumed_transcript() {
     assert_eq!(expected, history.raw_items());
 }
 
+#[tokio::test]
+async fn record_initial_history_restores_latest_persisted_agent_task() {
+    let (session, _turn_context) = make_session_and_context().await;
+    let expected = RegisteredAgentTask {
+        agent_runtime_id: "agent-123".to_string(),
+        task_id: "task-123".to_string(),
+        registered_at: "2026-03-23T12:00:00Z".to_string(),
+    };
+    let rollout_items = vec![
+        RolloutItem::SessionState(codex_protocol::protocol::SessionStateUpdate {
+            agent_task: Some(expected.to_session_agent_task()),
+        }),
+        RolloutItem::SessionState(codex_protocol::protocol::SessionStateUpdate {
+            agent_task: None,
+        }),
+        RolloutItem::SessionState(codex_protocol::protocol::SessionStateUpdate {
+            agent_task: Some(expected.to_session_agent_task()),
+        }),
+    ];
+
+    session
+        .record_initial_history(InitialHistory::Resumed(ResumedHistory {
+            conversation_id: ThreadId::default(),
+            history: rollout_items,
+            rollout_path: PathBuf::from("/tmp/resume.jsonl"),
+        }))
+        .await;
+
+    assert_eq!(session.state.lock().await.agent_task(), Some(expected));
+}
+
+#[tokio::test]
+async fn record_initial_history_honors_cleared_persisted_agent_task() {
+    let (session, _turn_context) = make_session_and_context().await;
+    let rollout_items = vec![
+        RolloutItem::SessionState(codex_protocol::protocol::SessionStateUpdate {
+            agent_task: Some(
+                RegisteredAgentTask {
+                    agent_runtime_id: "agent-123".to_string(),
+                    task_id: "task-123".to_string(),
+                    registered_at: "2026-03-23T12:00:00Z".to_string(),
+                }
+                .to_session_agent_task(),
+            ),
+        }),
+        RolloutItem::SessionState(codex_protocol::protocol::SessionStateUpdate {
+            agent_task: None,
+        }),
+    ];
+
+    session
+        .record_initial_history(InitialHistory::Resumed(ResumedHistory {
+            conversation_id: ThreadId::default(),
+            history: rollout_items,
+            rollout_path: PathBuf::from("/tmp/resume.jsonl"),
+        }))
+        .await;
+
+    assert_eq!(session.state.lock().await.agent_task(), None);
+}
+
 #[tokio::test]
 async fn record_initial_history_new_defers_initial_context_until_first_turn() {
     let (session, _turn_context) = make_session_and_context().await;
@@ -2954,6 +3015,7 @@ pub(crate) async fn make_session_and_context() -> (Session, TurnContext) {
         services,
         js_repl,
         next_internal_sub_id: AtomicU64::new(0),
+        agent_task_registration_lock: Mutex::new(()),
     };
 
     (session, turn_context)
@@ -3804,6 +3866,7 @@ pub(crate) async fn make_session_and_context_with_dynamic_tools_and_rx(
         services,
         js_repl,
         next_internal_sub_id: AtomicU64::new(0),
+        agent_task_registration_lock: Mutex::new(()),
     });
 
     (session, turn_context, rx_event)
diff --git a/codex-rs/core/src/state/session_tests.rs b/codex-rs/core/src/state/session_tests.rs
index 6816c8731d..d5ae7fcde6 100644
--- a/codex-rs/core/src/state/session_tests.rs
+++ b/codex-rs/core/src/state/session_tests.rs
@@ -39,10 +39,7 @@ async fn set_agent_task_persists_plaintext_task_for_session_reuse() {
     let session_configuration = make_session_configuration_for_tests().await;
     let mut state = SessionState::new(session_configuration);
     let agent_task = RegisteredAgentTask {
-        binding_id: "chatgpt-account-account-123".to_string(),
-        chatgpt_account_id: "account-123".to_string(),
-        chatgpt_user_id: Some("user-123".to_string()),
-        agent_runtime_id: "agent_123".to_string(),
+        agent_runtime_id: "agent-123".to_string(),
         task_id: "task_123".to_string(),
         registered_at: "2026-03-23T12:00:00Z".to_string(),
     };
@@ -57,9 +54,6 @@ async fn clear_agent_task_removes_cached_task() {
     let session_configuration = make_session_configuration_for_tests().await;
     let mut state = SessionState::new(session_configuration);
     let agent_task = RegisteredAgentTask {
-        binding_id: "chatgpt-account-account-123".to_string(),
-        chatgpt_account_id: "account-123".to_string(),
-        chatgpt_user_id: Some("user-123".to_string()),
         agent_runtime_id: "agent_123".to_string(),
         task_id: "task_123".to_string(),
         registered_at: "2026-03-23T12:00:00Z".to_string(),
diff --git a/codex-rs/protocol/src/protocol.rs b/codex-rs/protocol/src/protocol.rs
index 65d6dab04c..8fb4dc6138 100644
--- a/codex-rs/protocol/src/protocol.rs
+++ b/codex-rs/protocol/src/protocol.rs
@@ -2666,6 +2666,21 @@ impl fmt::Display for SubAgentSource {
     }
 }
 
+/// Persisted agent-task details that let a resumed thread keep using the same backend task.
+#[derive(Serialize, Deserialize, Clone, Debug, PartialEq, Eq, JsonSchema, TS)]
+pub struct SessionAgentTask {
+    pub agent_runtime_id: String,
+    pub task_id: String,
+    pub registered_at: String,
+}
+
+/// Session-scoped state updates that can be appended after the canonical SessionMeta line.
+#[derive(Serialize, Deserialize, Clone, Debug, PartialEq, Eq, JsonSchema, TS, Default)]
+pub struct SessionStateUpdate {
+    #[serde(default)]
+    pub agent_task: Option<SessionAgentTask>,
+}
+
 /// SessionMeta contains session-level data that doesn't correspond to a specific turn.
 ///
 /// NOTE: There used to be an `instructions` field here, which stored user_instructions, but we
@@ -2735,6 +2750,7 @@ pub struct SessionMetaLine {
 #[serde(tag = "type", content = "payload", rename_all = "snake_case")]
 pub enum RolloutItem {
     SessionMeta(SessionMetaLine),
+    SessionState(SessionStateUpdate),
     ResponseItem(ResponseItem),
     Compacted(CompactedItem),
     TurnContext(TurnContextItem),
diff --git a/codex-rs/rollout/src/list.rs b/codex-rs/rollout/src/list.rs
index e7d3dae5de..78510b8cac 100644
--- a/codex-rs/rollout/src/list.rs
+++ b/codex-rs/rollout/src/list.rs
@@ -1063,6 +1063,9 @@ async fn read_head_summary(path: &Path, head_limit: usize) -> io::Result<HeadTai
             RolloutItem::Compacted(_) => {
                 // Not included in `head`; skip.
             }
+            RolloutItem::SessionState(_) => {
+                // Not included in `head`; skip.
+            }
             RolloutItem::EventMsg(ev) => {
                 if let EventMsg::UserMessage(user) = ev {
                     summary.saw_user_event = true;
@@ -1115,6 +1118,7 @@ pub async fn read_head_for_summary(path: &Path) -> io::Result<Vec<serde_json::Va
                     }
                 }
                 RolloutItem::Compacted(_)
+                | RolloutItem::SessionState(_)
                 | RolloutItem::TurnContext(_)
                 | RolloutItem::EventMsg(_) => {}
             }
diff --git a/codex-rs/rollout/src/metadata.rs b/codex-rs/rollout/src/metadata.rs
index e8a95839d7..be920b79e2 100644
--- a/codex-rs/rollout/src/metadata.rs
+++ b/codex-rs/rollout/src/metadata.rs
@@ -70,7 +70,8 @@ pub fn builder_from_items(
 ) -> Option<ThreadMetadataBuilder> {
     if let Some(session_meta) = items.iter().find_map(|item| match item {
         RolloutItem::SessionMeta(meta_line) => Some(meta_line),
-        RolloutItem::ResponseItem(_)
+        RolloutItem::SessionState(_)
+        | RolloutItem::ResponseItem(_)
         | RolloutItem::Compacted(_)
         | RolloutItem::TurnContext(_)
         | RolloutItem::EventMsg(_) => None,
@@ -124,7 +125,8 @@ pub async fn extract_metadata_from_rollout(
         metadata,
         memory_mode: items.iter().rev().find_map(|item| match item {
             RolloutItem::SessionMeta(meta_line) => meta_line.meta.memory_mode.clone(),
-            RolloutItem::ResponseItem(_)
+            RolloutItem::SessionState(_)
+            | RolloutItem::ResponseItem(_)
             | RolloutItem::Compacted(_)
             | RolloutItem::TurnContext(_)
             | RolloutItem::EventMsg(_) => None,
diff --git a/codex-rs/rollout/src/policy.rs b/codex-rs/rollout/src/policy.rs
index 4b50781e76..6e6fb8b7a2 100644
--- a/codex-rs/rollout/src/policy.rs
+++ b/codex-rs/rollout/src/policy.rs
@@ -16,9 +16,10 @@ pub fn is_persisted_response_item(item: &RolloutItem, mode: EventPersistenceMode
         RolloutItem::ResponseItem(item) => should_persist_response_item(item),
         RolloutItem::EventMsg(ev) => should_persist_event_msg(ev, mode),
         // Persist Codex executive markers so we can analyze flows (e.g., compaction, API turns).
-        RolloutItem::Compacted(_) | RolloutItem::TurnContext(_) | RolloutItem::SessionMeta(_) => {
-            true
-        }
+        RolloutItem::Compacted(_)
+        | RolloutItem::TurnContext(_)
+        | RolloutItem::SessionMeta(_)
+        | RolloutItem::SessionState(_) => true,
     }
 }
 
diff --git a/codex-rs/rollout/src/recorder.rs b/codex-rs/rollout/src/recorder.rs
index 01ea10cb95..309865613c 100644
--- a/codex-rs/rollout/src/recorder.rs
+++ b/codex-rs/rollout/src/recorder.rs
@@ -683,6 +683,9 @@ impl RolloutRecorder {
                     RolloutItem::Compacted(item) => {
                         items.push(RolloutItem::Compacted(item));
                     }
+                    RolloutItem::SessionState(update) => {
+                        items.push(RolloutItem::SessionState(update));
+                    }
                     RolloutItem::TurnContext(item) => {
                         items.push(RolloutItem::TurnContext(item));
                     }
@@ -1303,6 +1306,7 @@ async fn resume_candidate_matches_cwd(
         && let Some(latest_turn_context_cwd) = items.iter().rev().find_map(|item| match item {
             RolloutItem::TurnContext(turn_context) => Some(turn_context.cwd.as_path()),
             RolloutItem::SessionMeta(_)
+            | RolloutItem::SessionState(_)
             | RolloutItem::ResponseItem(_)
             | RolloutItem::Compacted(_)
             | RolloutItem::EventMsg(_) => None,
diff --git a/codex-rs/state/src/extract.rs b/codex-rs/state/src/extract.rs
index 91c6755ffe..9294637361 100644
--- a/codex-rs/state/src/extract.rs
+++ b/codex-rs/state/src/extract.rs
@@ -19,6 +19,7 @@ pub fn apply_rollout_item(
 ) {
     match item {
         RolloutItem::SessionMeta(meta_line) => apply_session_meta_from_item(metadata, meta_line),
+        RolloutItem::SessionState(_) => {}
         RolloutItem::TurnContext(turn_ctx) => apply_turn_context(metadata, turn_ctx),
         RolloutItem::EventMsg(event) => apply_event_msg(metadata, event),
         RolloutItem::ResponseItem(item) => apply_response_item(metadata, item),
@@ -36,9 +37,10 @@ pub fn rollout_item_affects_thread_metadata(item: &RolloutItem) -> bool {
         RolloutItem::EventMsg(
             EventMsg::TokenCount(_) | EventMsg::UserMessage(_) | EventMsg::ThreadNameUpdated(_),
         ) => true,
-        RolloutItem::EventMsg(_) | RolloutItem::ResponseItem(_) | RolloutItem::Compacted(_) => {
-            false
-        }
+        RolloutItem::SessionState(_)
+        | RolloutItem::EventMsg(_)
+        | RolloutItem::ResponseItem(_)
+        | RolloutItem::Compacted(_) => false,
     }
 }
 
diff --git a/codex-rs/state/src/runtime/threads.rs b/codex-rs/state/src/runtime/threads.rs
index e56ca3f386..0ae73bcc14 100644
--- a/codex-rs/state/src/runtime/threads.rs
+++ b/codex-rs/state/src/runtime/threads.rs
@@ -912,7 +912,8 @@ fn one_thread_id_from_rows(
 pub(super) fn extract_dynamic_tools(items: &[RolloutItem]) -> Option<Option<Vec<DynamicToolSpec>>> {
     items.iter().find_map(|item| match item {
         RolloutItem::SessionMeta(meta_line) => Some(meta_line.meta.dynamic_tools.clone()),
-        RolloutItem::ResponseItem(_)
+        RolloutItem::SessionState(_)
+        | RolloutItem::ResponseItem(_)
         | RolloutItem::Compacted(_)
         | RolloutItem::TurnContext(_)
         | RolloutItem::EventMsg(_) => None,
@@ -922,7 +923,8 @@ pub(super) fn extract_dynamic_tools(items: &[RolloutItem]) -> Option<Option<Vec<
 pub(super) fn extract_memory_mode(items: &[RolloutItem]) -> Option<String> {
     items.iter().rev().find_map(|item| match item {
         RolloutItem::SessionMeta(meta_line) => meta_line.meta.memory_mode.clone(),
-        RolloutItem::ResponseItem(_)
+        RolloutItem::SessionState(_)
+        | RolloutItem::ResponseItem(_)
         | RolloutItem::Compacted(_)
         | RolloutItem::TurnContext(_)
         | RolloutItem::EventMsg(_) => None,
diff --git a/notes/pr17387-agent-task-persistence-assumption.md b/notes/pr17387-agent-task-persistence-assumption.md
new file mode 100644
index 0000000000..9b1059ebbc
--- /dev/null
+++ b/notes/pr17387-agent-task-persistence-assumption.md
@@ -0,0 +1,15 @@
+# PR 17387 Agent Task Persistence Assumption
+
+The review request said to persist the registered agent task_id "in the same place that other
+session details are stored" without specifying the exact persistence shape.
+
+Assumption used in this patch:
+
+- Persist session-scoped agent task state in the thread rollout file, alongside other resumable
+  thread/session data.
+- Keep agent identity registration on startup, but register the backend task lazily when a session
+  first needs task-scoped auth.
+- Model task updates as an append-only RolloutItem::SessionState record instead of mutating the
+  canonical first SessionMeta line, because resumed threads need later updates and clears to win.
+- Do not carry auth-binding fields on the persisted session task; only persist the task fields
+  needed to resume the same backend task for the same stored registered agent identity.