diff --git a/gateway/platforms/api_server_openai_routes.py b/gateway/platforms/api_server_openai_routes.py
index 991a5d74c6..db2edf0ac2 100644
--- a/gateway/platforms/api_server_openai_routes.py
+++ b/gateway/platforms/api_server_openai_routes.py
@@ -88,6 +88,37 @@ def _message_item(text: Any) -> Dict[str, Any]:
             "content": [{"type": "output_text", "text": text}]}
 
 
+def _reasoning_item(text: str) -> Dict[str, Any]:
+    """Completed Responses ``reasoning`` output item (same shape the SSE writer closes with)."""
+    return {"id": f"rs_{uuid.uuid4().hex[:24]}", "type": "reasoning", "status": "completed",
+            "summary": [{"type": "summary_text", "text": text}]}
+
+
+def _is_reasoning_input_item(item: Any) -> bool:
+    """Echoed-back ``reasoning`` output item: Responses SDK clients replay a prior response's
+    ``output`` list as the next ``input``. It carries no message content, so it must be
+    skipped rather than parsed into an empty ``user`` turn (#99552)."""
+    return isinstance(item, dict) and item.get("type") == "reasoning"
+
+
+def _turn_reasoning_text(
+        conversation_history: List[Dict[str, Any]], user_message: Any, result: Dict[str, Any]) -> str:
+    """Reasoning the model produced on this turn, joined for a non-streaming
+    ``message.reasoning_content``. Read from the assistant messages the agent already
+    persisted (``build_assistant_message`` stores the structured reasoning under
+    ``reasoning``) rather than re-accumulating callback deltas, so it is exactly what the
+    stream would have carried and cannot double-count the post-response fallback."""
+    messages = result.get("messages") if isinstance(result, dict) else None
+    if not isinstance(messages, list):
+        return ""
+    start = OpenAICompatRoutesMixin._response_messages_turn_start_index(
+        conversation_history, user_message, result)
+    parts = [m["reasoning"] for m in messages[start:]
+             if isinstance(m, dict) and m.get("role") == "assistant"
+             and isinstance(m.get("reasoning"), str) and m["reasoning"].strip()]
+    return "\n\n".join(parts)
+
+
 def _trim_tool_items(items: List[Dict[str, Any]]) -> List[Dict[str, Any]]:
     """Trim large tool payloads in place so response.completed stays under ~100KB (clients
     already received the full details via the incremental events)."""
@@ -256,7 +287,7 @@ class _ResponsesStream:
         await self.write_event("response.reasoning_summary_part.done", {
             "type": "response.reasoning_summary_part.done", **base,
             "part": {"type": "summary_text", "text": text}})
-        self.emitted_items.append({"type": "reasoning", "summary": item["summary"]})
+        self.emitted_items.append(item)
         await self.write_event("response.output_item.done", {
             "type": "response.output_item.done", "output_index": rs["output_index"], "item": item})
 
@@ -645,6 +676,10 @@ class OpenAICompatRoutesMixin:
             "choices": [{"index": 0, "message": {"role": "assistant", "content": "" if presentation_muted else final_response},
                          "finish_reason": finish_reason}],
             "usage": _chat_usage_payload(usage)}
+        # Non-streaming twin of ``delta.reasoning_content`` (#99552).
+        reasoning_text = _turn_reasoning_text(history, user_message, result)
+        if reasoning_text and not presentation_muted:
+            response_data["choices"][0]["message"]["reasoning_content"] = reasoning_text
         if is_partial or is_failed or not completed:
             response_data["hermes"] = _hermes_extras(
                 completed, is_partial, is_failed, "" if presentation_muted else err_msg, finish_reason)
@@ -867,6 +902,8 @@ class OpenAICompatRoutesMixin:
             for idx, item in enumerate(raw_input):
                 if isinstance(item, str):
                     input_messages.append({"role": "user", "content": item})
+                elif _is_reasoning_input_item(item):
+                    continue
                 elif isinstance(item, dict):
                     try:
                         content = _normalize_multimodal_content(item.get("content", ""))
@@ -883,6 +920,8 @@ class OpenAICompatRoutesMixin:
             if not isinstance(raw_history, list):
                 return _error_response("'conversation_history' must be an array of message objects", 400)
             for i, entry in enumerate(raw_history):
+                if _is_reasoning_input_item(entry):
+                    continue
                 if not isinstance(entry, dict) or "role" not in entry or "content" not in entry:
                     return _error_response(f"conversation_history[{i}] must have 'role' and 'content' fields", 400)
                 try:
@@ -1096,6 +1135,11 @@ class OpenAICompatRoutesMixin:
             messages = messages[start_index:]
         for msg in messages:
             role = msg.get("role")
+            reasoning = msg.get("reasoning") if role == "assistant" else None
+            if isinstance(reasoning, str) and reasoning.strip():
+                # Precedes this message's function_call items, like the SSE writer closes a
+                # thinking burst before the next tool item opens (#99552).
+                items.append(_reasoning_item(reasoning))
             if role == "assistant" and msg.get("tool_calls"):
                 for tc in msg["tool_calls"]:
                     func = tc.get("function", {})
diff --git a/tests/gateway/test_api_server_reasoning_nonstream.py b/tests/gateway/test_api_server_reasoning_nonstream.py
new file mode 100644
index 0000000000..33244a98e4
--- /dev/null
+++ b/tests/gateway/test_api_server_reasoning_nonstream.py
@@ -0,0 +1,93 @@
+"""Reasoning on the non-streaming OpenAI-compatible routes and the Responses input parser (#99552).
+
+Non-streaming ``/v1/chat/completions`` carries ``message.reasoning_content`` and non-streaming
+``/v1/responses`` a ``reasoning`` output item, read from the assistant messages the agent
+persisted; a client replaying a prior response's output list (its ``reasoning`` item included)
+as the next ``input`` / ``conversation_history`` must not get a 400 or an empty user turn.
+"""
+
+from unittest.mock import patch
+
+import pytest
+from aiohttp import web
+from aiohttp.test_utils import TestClient, TestServer
+
+from gateway.config import PlatformConfig
+from gateway.platforms.api_server import APIServerAdapter
+
+REASONING = "Let me think about this carefully."
+
+
+def _result(user_text: str) -> dict:
+    """Transcript-shaped agent result whose assistant message carries structured reasoning."""
+    return {"final_response": "42", "completed": True,
+            "messages": [{"role": "user", "content": user_text},
+                         {"role": "assistant", "content": "42", "reasoning": REASONING}]}
+
+
+def _app() -> tuple:
+    adapter = APIServerAdapter(PlatformConfig(enabled=True, extra={}))
+    app = web.Application()
+    app["api_server_adapter"] = adapter
+    app.router.add_post("/v1/chat/completions", adapter._handle_chat_completions)
+    app.router.add_post("/v1/responses", adapter._handle_responses)
+    app.router.add_get("/v1/responses/{response_id}", adapter._handle_get_response)
+    return TestClient(TestServer(app)), adapter
+
+
+@pytest.mark.asyncio
+async def test_non_streaming_routes_carry_reasoning_once():
+    """Non-stream chat: ``message.reasoning_content`` equals the persisted reasoning exactly
+    (no delta+fallback doubling); non-stream responses: one completed ``reasoning`` item
+    before the message, also present on ``GET /v1/responses/{id}`` replay."""
+    client, adapter = _app()
+    async with client:
+        async def _fake_run_agent(**kw):
+            return _result(kw["user_message"]), {"input_tokens": 1, "output_tokens": 1, "total_tokens": 2}
+
+        with patch.object(adapter, "_run_agent", side_effect=_fake_run_agent):
+            r = await client.post("/v1/chat/completions", json={
+                "model": "hermes-agent", "messages": [{"role": "user", "content": "q"}]})
+            assert r.status == 200
+            message = (await r.json())["choices"][0]["message"]
+            assert message["reasoning_content"] == REASONING
+            assert REASONING not in message["content"]
+
+            r = await client.post("/v1/responses", json={"model": "hermes-agent", "input": "q", "store": True})
+            assert r.status == 200
+            data = await r.json()
+            assert [o["type"] for o in data["output"]] == ["reasoning", "message"]
+            assert data["output"][0]["status"] == "completed"
+            assert data["output"][0]["summary"] == [{"type": "summary_text", "text": REASONING}]
+            replay = await (await client.get(f"/v1/responses/{data['id']}")).json()
+            assert [o["type"] for o in replay["output"]] == ["reasoning", "message"]
+
+
+@pytest.mark.asyncio
+async def test_responses_input_ignores_echoed_reasoning_items():
+    """A ``{type: reasoning}`` item replayed in ``input`` or ``conversation_history`` is skipped:
+    no 400, no empty ``user`` message in the history the agent receives."""
+    client, adapter = _app()
+    async with client:
+        captured = {}
+
+        async def _fake_run_agent(**kw):
+            captured["history"] = kw["conversation_history"]
+            captured["user"] = kw["user_message"]
+            return _result(kw["user_message"]), {}
+
+        reasoning_item = {"type": "reasoning", "id": "rs_1",
+                          "summary": [{"type": "summary_text", "text": "thought"}]}
+        with patch.object(adapter, "_run_agent", side_effect=_fake_run_agent):
+            r = await client.post("/v1/responses", json={
+                "model": "hermes-agent", "store": False,
+                "conversation_history": [{"role": "user", "content": "h0"}, reasoning_item,
+                                         {"role": "assistant", "content": "a0"}],
+                "input": [{"role": "user", "content": "first"}, reasoning_item,
+                          {"type": "message", "role": "assistant",
+                           "content": [{"type": "output_text", "text": "hi"}]},
+                          {"role": "user", "content": "second"}]})
+        assert r.status == 200, await r.text()
+        assert captured["user"] == "second"
+        assert [(m["role"], m["content"]) for m in captured["history"]] == [
+            ("user", "h0"), ("assistant", "a0"), ("user", "first"), ("assistant", "hi")]
diff --git a/website/docs/user-guide/features/api-server.md b/website/docs/user-guide/features/api-server.md
index e0d49ebc82..925f055b39 100644
--- a/website/docs/user-guide/features/api-server.md
+++ b/website/docs/user-guide/features/api-server.md
@@ -114,10 +114,12 @@ All SSE streams (Chat Completions, Responses, `/api/sessions/{id}/chat/stream`,
 - **Chat Completions**: Hermes emits `event: hermes.tool.progress` for tool-start visibility without polluting persisted assistant text.
 - **Responses**: Hermes emits spec-native `function_call` and `function_call_output` output items during the SSE stream, so clients can render structured tool UI in real time.
 
-**Model reasoning in streams** (emitted only when the model actually produces reasoning and the resolved `reasoning` config allows it; the input-side opt-out is `model_options.reasoning.enabled: false`):
+**Model reasoning** (emitted only when the model actually produces reasoning and the resolved `reasoning` config allows it; the input-side opt-out is `model_options.reasoning.enabled: false`):
 - **Chat Completions**: reasoning deltas arrive as `choices[0].delta.reasoning_content` chunks (the DeepSeek-style field Open WebUI, opencode and the Vercel AI SDK render as a thinking block); answer text stays in `delta.content`.
-- **Responses**: each thinking burst is a spec-native `reasoning` output item — `response.output_item.added` (`item.type: "reasoning"`), `response.reasoning_summary_part.added`, `response.reasoning_summary_text.delta` … `response.reasoning_summary_text.done`, `response.reasoning_summary_part.done`, `response.output_item.done` — closed before the next message or `function_call` item opens, and echoed in the `response.completed` output as `{"type": "reasoning", "summary": [{"type": "summary_text", "text": "…"}]}`. `sequence_number` stays monotonic across reasoning, text and tool events.
-- Support is advertised as `features.reasoning_streaming: true` on `GET /v1/capabilities`. Non-streaming responses do not carry reasoning.
+- **Responses**: each thinking burst is a spec-native `reasoning` output item — `response.output_item.added` (`item.type: "reasoning"`), `response.reasoning_summary_part.added`, `response.reasoning_summary_text.delta` … `response.reasoning_summary_text.done`, `response.reasoning_summary_part.done`, `response.output_item.done` — closed before the next message or `function_call` item opens, and echoed in the `response.completed` output as `{"id": "rs_…", "type": "reasoning", "status": "completed", "summary": [{"type": "summary_text", "text": "…"}]}`. `sequence_number` stays monotonic across reasoning, text and tool events.
+- **Non-streaming**: `/v1/chat/completions` returns the turn's reasoning on `choices[0].message.reasoning_content`; `/v1/responses` returns the same `reasoning` output item(s) ahead of the message (and of that step's `function_call` items), also on `GET /v1/responses/{id}` replay.
+- Echoing a prior response's `output` list back as the next `input` (what Responses SDK clients do) is fine: `reasoning` items are ignored on input rather than parsed as empty user turns.
+- Support is advertised as `features.reasoning_streaming: true` on `GET /v1/capabilities`.
 
 ### POST /v1/responses