diff --git a/tensorrt_llm/serve/responses_utils.py b/tensorrt_llm/serve/responses_utils.py
index edd36f8624f9..9c2aa65db867 100644
--- a/tensorrt_llm/serve/responses_utils.py
+++ b/tensorrt_llm/serve/responses_utils.py
@@ -257,9 +257,6 @@ async def store_response(self,
 
                 conversation_id = self.response_to_conversation[prev_resp_id]
                 self.conversations[conversation_id].extend(resp_msgs)
-                while len(self.conversations[conversation_id]
-                          ) > self.conversation_capacity:
-                    self._pop_conversation(resp_id)
             else:
                 conversation_id = _random_uuid()
                 self.conversations[conversation_id] = resp_msgs
@@ -269,6 +266,7 @@ async def store_response(self,
 
             self.response_to_conversation[resp_id] = conversation_id
             self.conversation_to_response[conversation_id] = resp_id
+            self._trim_conversation(conversation_id)
             self._update_visited_conversation(conversation_id)
 
     async def pop_response(self, resp_id: Optional[str] = None) -> bool:
@@ -307,12 +305,10 @@ async def store_messages(self, resp_id: str,
             _responses_debug_log(
                 f" * storing at conversation: {conversation_id}")
             self.conversations[conversation_id] = msgs
-            if len(self.conversations[conversation_id]
-                   ) > self.conversation_capacity:
-                self._pop_conversation(resp_id)
 
             self.response_to_conversation[resp_id] = conversation_id
             self.conversation_to_response[conversation_id] = resp_id
+            self._trim_conversation(conversation_id)
             self._update_visited_conversation(conversation_id)
 
     async def get_conversation_history(
@@ -372,8 +368,20 @@ def _pop_conversation(self, resp_id) -> None:
         if conversation_id is None:
             return
 
-        conversation = self.conversations[conversation_id]
-        if len(conversation) == 0:
+        self._pop_conversation_by_conversation_id(conversation_id)
+
+    def _trim_conversation(self, conversation_id: str) -> None:
+        conversation = self.conversations.get(conversation_id)
+        if conversation is None:
+            return
+
+        while len(conversation) > self.conversation_capacity:
+            self._pop_conversation_by_conversation_id(conversation_id)
+
+    def _pop_conversation_by_conversation_id(self,
+                                             conversation_id: str) -> None:
+        conversation = self.conversations.get(conversation_id)
+        if conversation is None or len(conversation) == 0:
             return
 
         is_harmony_conversation = isinstance(conversation[0], Message)
diff --git a/tests/unittest/llmapi/test_responses_utils.py b/tests/unittest/llmapi/test_responses_utils.py
new file mode 100644
index 000000000000..7b1a413cea82
--- /dev/null
+++ b/tests/unittest/llmapi/test_responses_utils.py
@@ -0,0 +1,89 @@
+# SPDX-FileCopyrightText: Copyright (c) 2026 NVIDIA CORPORATION & AFFILIATES. All rights reserved.
+# SPDX-License-Identifier: Apache-2.0
+#
+# Licensed under the Apache License, Version 2.0 (the "License");
+# you may not use this file except in compliance with the License.
+# You may obtain a copy of the License at
+#
+# http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software
+# distributed under the License is distributed on an "AS IS" BASIS,
+# WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+# See the License for the specific language governing permissions and
+# limitations under the License.
+
+from types import SimpleNamespace
+
+import pytest
+
+from tensorrt_llm.serve.responses_utils import ConversationHistoryStore
+
+
+def _turns(count: int):
+    messages = []
+    for index in range(count):
+        messages.extend(
+            [
+                {
+                    "role": "user",
+                    "content": f"user {index}",
+                },
+                {
+                    "role": "assistant",
+                    "content": f"assistant {index}",
+                },
+            ]
+        )
+    return messages
+
+
+@pytest.mark.asyncio
+async def test_store_response_trims_pre_stored_request_conversation():
+    store = ConversationHistoryStore(resp_capacity=1)
+
+    await store.store_messages("resp_1", _turns(3), prev_resp_id=None)
+    await store.store_response(
+        SimpleNamespace(id="resp_1"),
+        [
+            {
+                "role": "assistant",
+                "content": "final",
+            }
+        ],
+        prev_resp_id=None,
+    )
+
+    conversation = await store.get_conversation_history("resp_1")
+
+    assert len(conversation) <= store.conversation_capacity
+
+
+@pytest.mark.asyncio
+async def test_store_response_trims_previous_response_conversation(monkeypatch):
+    store = ConversationHistoryStore(resp_capacity=1)
+
+    await store.store_messages("resp_prev", _turns(2), prev_resp_id=None)
+
+    def fail_if_unmapped_response_id_is_used(_):
+        raise AssertionError("conversation trim used an unmapped response id")
+
+    monkeypatch.setattr(store, "_pop_conversation", fail_if_unmapped_response_id_is_used)
+
+    await store.store_response(
+        SimpleNamespace(id="resp_next"),
+        [
+            {
+                "role": "assistant",
+                "content": "next",
+            }
+        ],
+        prev_resp_id="resp_prev",
+    )
+
+    conversation = await store.get_conversation_history("resp_next")
+
+    assert len(conversation) <= store.conversation_capacity
+    assert (
+        store.response_to_conversation["resp_next"] == store.response_to_conversation["resp_prev"]
+    )