diff --git a/codex-rs/core/src/agent/control/spawn.rs b/codex-rs/core/src/agent/control/spawn.rs
index c116542433..6eae0d3887 100644
--- a/codex-rs/core/src/agent/control/spawn.rs
+++ b/codex-rs/core/src/agent/control/spawn.rs
@@ -8,6 +8,8 @@ use crate::context::ManagedDeveloperInstructions;
 use crate::context::MultiAgentModeInstructions;
 use crate::context::MultiAgentRoleInstructions;
 use crate::session::multi_agents::resolve_usage_hints;
+use codex_context_fragments::set_annotated_content;
+use codex_context_fragments::to_annotated_content;
 use codex_extension_api::ExtensionDataInit;
 
 const AGENT_NAMES: &str = include_str!("../agent_names.txt");
@@ -91,15 +93,15 @@ fn keep_forked_rollout_item(item: &RolloutItem, preserve_reference_context_item:
 }
 
 fn retain_forked_developer_message(item: &mut ResponseItem, usage_hint_texts: &[String]) -> bool {
-    let ResponseItem::Message { role, content, .. } = item else {
-        return true;
-    };
-    if role != "developer" {
+    if !matches!(item, ResponseItem::Message { role, .. } if role == "developer") {
         return true;
     }
 
+    let Some(mut content) = to_annotated_content(item) else {
+        return false;
+    };
     content.retain(|content_item| {
-        let ContentItem::InputText { text } = content_item else {
+        let ContentItem::InputText { text } = content_item.content() else {
             return true;
         };
 
@@ -110,7 +112,7 @@ fn retain_forked_developer_message(item: &mut ResponseItem, usage_hint_texts: &[
                 .iter()
                 .any(|usage_hint_text| usage_hint_text == text))
     });
-    !content.is_empty()
+    !content.is_empty() && set_annotated_content(item, content).is_some()
 }
 
 async fn load_agent_model_context(
@@ -741,11 +743,12 @@ impl AgentControl {
                 return false;
             }
 
-            if let ResponseItem::Message { role, content, .. } = response_item
-                && role == "developer"
-            {
+            if matches!(response_item, ResponseItem::Message { role, .. } if role == "developer") {
+                let Some(mut content) = to_annotated_content(response_item) else {
+                    return false;
+                };
                 content.retain_mut(|content_item| {
-                    let ContentItem::InputText { text } = content_item else {
+                    let ContentItem::InputText { text } = content_item.content_mut() else {
                         return true;
                     };
                     if ManagedDeveloperInstructions::matches_text(text) {
@@ -777,7 +780,8 @@ impl AgentControl {
                     *text = text.replace(parent_developer_instructions, replacement);
                     !text.is_empty()
                 });
-                return !content.is_empty();
+                return !content.is_empty()
+                    && set_annotated_content(response_item, content).is_some();
             }
 
             true
diff --git a/codex-rs/core/src/agent/control_tests.rs b/codex-rs/core/src/agent/control_tests.rs
index b706a412c6..882b39488d 100644
--- a/codex-rs/core/src/agent/control_tests.rs
+++ b/codex-rs/core/src/agent/control_tests.rs
@@ -35,7 +35,9 @@ use codex_protocol::error::CodexErrorDetails;
 use codex_protocol::items::TurnItem;
 use codex_protocol::items::UserMessageItem;
 use codex_protocol::models::ContentItem;
+use codex_protocol::models::ContentItemKind;
 use codex_protocol::models::FunctionCallOutputPayload;
+use codex_protocol::models::InternalChatMessageMetadataPassthrough;
 use codex_protocol::models::MessagePhase;
 use codex_protocol::models::PermissionProfile;
 use codex_protocol::models::ResponseItem;
@@ -1404,7 +1406,17 @@ async fn spawn_agent_can_fork_parent_thread_history_with_sanitized_items() {
                         },
                     ],
                     phase: None,
-                    internal_chat_message_metadata_passthrough: None,
+                    internal_chat_message_metadata_passthrough: Some(
+                        InternalChatMessageMetadataPassthrough {
+                            content_item_kinds: Some(vec![
+                                ContentItemKind("generic.developer_instructions".to_string()),
+                                ContentItemKind("multi_agent.mode_instructions".to_string()),
+                                ContentItemKind("generic.developer_policy".to_string()),
+                                ContentItemKind("managed_config.developer_instructions".to_string()),
+                            ]),
+                            ..Default::default()
+                        },
+                    ),
                 },
                 assistant_message("parent commentary", Some(MessagePhase::Commentary)),
                 assistant_message("parent final answer", Some(MessagePhase::FinalAnswer)),
@@ -1499,7 +1511,16 @@ async fn spawn_agent_can_fork_parent_thread_history_with_sanitized_items() {
             },
         ],
         phase: None,
-        internal_chat_message_metadata_passthrough: None,
+        internal_chat_message_metadata_passthrough: Some(
+            InternalChatMessageMetadataPassthrough {
+                content_item_kinds: Some(vec![
+                    ContentItemKind("generic.developer_instructions".to_string()),
+                    ContentItemKind("generic.developer_policy".to_string()),
+                    ContentItemKind("managed_config.developer_instructions".to_string()),
+                ]),
+                ..Default::default()
+            },
+        ),
     };
     expected_developer_message.set_turn_id_if_missing(&turn_context.sub_id);
     expected_developer_message.set_create_time_if_missing(
diff --git a/codex-rs/core/tests/suite/subagent_notifications.rs b/codex-rs/core/tests/suite/subagent_notifications.rs
index 484cf3e079..9ffa69d844 100644
--- a/codex-rs/core/tests/suite/subagent_notifications.rs
+++ b/codex-rs/core/tests/suite/subagent_notifications.rs
@@ -1328,6 +1328,20 @@ async fn spawned_full_history_v2_child_uses_model_precedence_without_dropping_co
 
     let child_request = wait_for_request_with_model(&child_request_log, expected_model).await?;
     assert!(child_request.body_contains_text(TURN_0_FORK_PROMPT));
+    let misaligned_child_messages = child_request
+        .inputs_of_type("message")
+        .into_iter()
+        .filter(|message| {
+            message["internal_chat_message_metadata_passthrough"]["content_item_kinds"]
+                .as_array()
+                .is_some_and(|kinds| {
+                    message["content"]
+                        .as_array()
+                        .is_none_or(|content| content.len() != kinds.len())
+                })
+        })
+        .collect::<Vec<_>>();
+    assert_eq!(misaligned_child_messages, Vec::<Value>::new());
     let child_developer_messages = child_request.message_input_texts("developer");
     if !matches!(
         selection,