diff --git a/agent/codex_responses_adapter.py b/agent/codex_responses_adapter.py
index e25293d7320..edb63849cb7 100644
--- a/agent/codex_responses_adapter.py
+++ b/agent/codex_responses_adapter.py
@@ -314,6 +314,7 @@ def _chat_messages_to_responses_input(
     messages: List[Dict[str, Any]],
     *,
     is_xai_responses: bool = False,
+    is_github_responses: bool = False,
     replay_encrypted_reasoning: bool = True,
     current_issuer_kind: Optional[str] = None,
 ) -> List[Dict[str, Any]]:
@@ -338,6 +339,16 @@ def _chat_messages_to_responses_input(
     items from the conversation history and threads ``replay_enabled=False``
     through this converter so subsequent turns send no reasoning items.
 
+    ``is_github_responses`` drops the ``id`` field from replayed
+    ``codex_message_items`` regardless of length. The Copilot backend
+    (api.githubcopilot.com/responses) binds these ids to a specific
+    backend "connection" — credential-pool rotation, a gateway restart,
+    or routine load-balancer churn between turns all invalidate it — and
+    rejects a stale id with HTTP 401 "input item ID does not belong to
+    this connection" even for short ids (see #32716). ``phase``/
+    ``status``/``content`` are still replayed; only ``id`` is unsafe to
+    reuse across a Copilot connection.
+
     ``current_issuer_kind`` enables a per-item cross-issuer guard. The
     Responses API's ``encrypted_content`` blob is decryptable only by the
     endpoint that minted it — replaying a Codex-issued blob against xAI
@@ -470,7 +481,11 @@ def _chat_messages_to_responses_input(
                             "content": normalized_content_parts,
                         }
                         item_id = raw_item.get("id")
-                        if isinstance(item_id, str) and item_id.strip():
+                        if (
+                            not is_github_responses
+                            and isinstance(item_id, str)
+                            and item_id.strip()
+                        ):
                             stripped_id = item_id.strip()
                             if len(stripped_id) <= _MAX_RESPONSES_ITEM_ID_LENGTH:
                                 replay_item["id"] = stripped_id
diff --git a/agent/transports/codex.py b/agent/transports/codex.py
index 56374b87533..ea78c97b9f6 100644
--- a/agent/transports/codex.py
+++ b/agent/transports/codex.py
@@ -81,6 +81,7 @@ class ResponsesApiTransport(ProviderTransport):
         return _chat_messages_to_responses_input(
             messages,
             is_xai_responses=bool(kwargs.get("is_xai_responses")),
+            is_github_responses=bool(kwargs.get("is_github_responses")),
             replay_encrypted_reasoning=bool(
                 kwargs.get("replay_encrypted_reasoning", True)
             ),
@@ -239,6 +240,7 @@ class ResponsesApiTransport(ProviderTransport):
             "input": _chat_messages_to_responses_input(
                 payload_messages,
                 is_xai_responses=is_xai_responses,
+                is_github_responses=is_github_responses,
                 replay_encrypted_reasoning=replay_encrypted_reasoning,
                 current_issuer_kind=issuer_kind,
             ),
diff --git a/tests/agent/transports/test_codex_transport.py b/tests/agent/transports/test_codex_transport.py
index 6389890519a..6116d3978fb 100644
--- a/tests/agent/transports/test_codex_transport.py
+++ b/tests/agent/transports/test_codex_transport.py
@@ -121,6 +121,63 @@ class TestCodexBuildKwargs:
         )
         assert "prompt_cache_key" not in kw
 
+    def test_github_responses_drops_message_item_id_end_to_end(self, transport):
+        # #32716: Copilot binds codex_message_items ids to a backend
+        # "connection" that doesn't survive credential rotation, a gateway
+        # restart, or load-balancer churn — replaying a stale id gets HTTP
+        # 401 "input item ID does not belong to this connection", even for
+        # ids well under the #27038 64-char length cap. build_kwargs must
+        # thread is_github_responses through to the input converter so the
+        # id never reaches the request.
+        messages = [
+            {"role": "system", "content": "You are Hermes."},
+            {
+                "role": "assistant",
+                "content": "pong",
+                "codex_message_items": [
+                    {
+                        "type": "message",
+                        "role": "assistant",
+                        "status": "completed",
+                        "content": [{"type": "output_text", "text": "pong"}],
+                        "id": "msg_short_but_connection_scoped",
+                        "phase": "final_answer",
+                    }
+                ],
+            },
+        ]
+        kw = transport.build_kwargs(
+            model="gpt-5.5", messages=messages, tools=[],
+            is_github_responses=True,
+        )
+        message_item = next(item for item in kw["input"] if item.get("type") == "message")
+        assert "id" not in message_item
+        assert message_item["phase"] == "final_answer"
+
+    def test_non_github_responses_keeps_message_item_id_end_to_end(self, transport):
+        messages = [
+            {"role": "system", "content": "You are Hermes."},
+            {
+                "role": "assistant",
+                "content": "pong",
+                "codex_message_items": [
+                    {
+                        "type": "message",
+                        "role": "assistant",
+                        "status": "completed",
+                        "content": [{"type": "output_text", "text": "pong"}],
+                        "id": "msg_short_id",
+                    }
+                ],
+            },
+        ]
+        kw = transport.build_kwargs(
+            model="gpt-5.5", messages=messages, tools=[],
+            is_codex_backend=True,
+        )
+        message_item = next(item for item in kw["input"] if item.get("type") == "message")
+        assert message_item["id"] == "msg_short_id"
+
     def test_xai_responses_sends_cache_key_via_extra_body(self, transport):
         """xAI's Responses API documents ``prompt_cache_key`` as the
         body-level cache-routing key (the ``x-grok-conv-id`` header is