diff --git a/letta/agents/helpers.py b/letta/agents/helpers.py
index 3e5aed0a..5cddbb89 100644
--- a/letta/agents/helpers.py
+++ b/letta/agents/helpers.py
@@ -144,7 +144,7 @@ async def _prepare_in_context_messages_no_persist_async(
         current_in_context_messages = await message_manager.get_messages_by_ids_async(message_ids=agent_state.message_ids, actor=actor)
 
     # Check for approval-related message validation
-    if len(input_messages) == 1 and input_messages[0].type == "approval":
+    if input_messages[0].type == "approval":
         # User is trying to send an approval response
         if current_in_context_messages and current_in_context_messages[-1].role != "approval":
             raise ValueError(
@@ -155,6 +155,11 @@ async def _prepare_in_context_messages_no_persist_async(
         new_in_context_messages = create_approval_response_message_from_input(
             agent_state=agent_state, input_message=input_messages[0], run_id=run_id
         )
+        if len(input_messages) > 1:
+            follow_up_messages = await create_input_messages(
+                input_messages=input_messages[1:], agent_id=agent_state.id, timezone=agent_state.timezone, run_id=run_id, actor=actor
+            )
+            new_in_context_messages.extend(follow_up_messages)
     else:
         # User is trying to send a regular message
         if current_in_context_messages and current_in_context_messages[-1].role == "approval":
diff --git a/letta/agents/letta_agent_v3.py b/letta/agents/letta_agent_v3.py
index 58e1fd5e..09b35fa5 100644
--- a/letta/agents/letta_agent_v3.py
+++ b/letta/agents/letta_agent_v3.py
@@ -114,9 +114,17 @@ class LettaAgentV3(LettaAgentV2):
         in_context_messages, input_messages_to_persist = await _prepare_in_context_messages_no_persist_async(
             input_messages, self.agent_state, self.message_manager, self.actor, run_id
         )
+        follow_up_messages = []
+        if len(input_messages_to_persist) > 1 and input_messages_to_persist[0].role == "approval":
+            follow_up_messages = input_messages_to_persist[1:]
+            input_messages_to_persist = [input_messages_to_persist[0]]
+
         in_context_messages = in_context_messages + input_messages_to_persist
         response_letta_messages = []
         for i in range(max_steps):
+            if i == 1 and follow_up_messages:
+                input_messages_to_persist = follow_up_messages
+                follow_up_messages = []
             response = self._step(
                 messages=in_context_messages + self.response_messages,
                 input_messages_to_persist=input_messages_to_persist,
@@ -237,8 +245,16 @@ class LettaAgentV3(LettaAgentV2):
             in_context_messages, input_messages_to_persist = await _prepare_in_context_messages_no_persist_async(
                 input_messages, self.agent_state, self.message_manager, self.actor, run_id
             )
+            follow_up_messages = []
+            if len(input_messages_to_persist) > 1 and input_messages_to_persist[0].role == "approval":
+                follow_up_messages = input_messages_to_persist[1:]
+                input_messages_to_persist = [input_messages_to_persist[0]]
+
             in_context_messages = in_context_messages + input_messages_to_persist
             for i in range(max_steps):
+                if i == 1 and follow_up_messages:
+                    input_messages_to_persist = follow_up_messages
+                    follow_up_messages = []
                 response = self._step(
                     messages=in_context_messages + self.response_messages,
                     input_messages_to_persist=input_messages_to_persist,
diff --git a/tests/integration_test_human_in_the_loop.py b/tests/integration_test_human_in_the_loop.py
index 9a007f61..0f02b9ef 100644
--- a/tests/integration_test_human_in_the_loop.py
+++ b/tests/integration_test_human_in_the_loop.py
@@ -585,6 +585,51 @@ def test_approve_and_follow_up_with_error(
         assert messages[2].message_type == "tool_return_message"
 
 
+def test_approve_with_user_message(
+    client: Letta,
+    agent: AgentState,
+) -> None:
+    response = client.agents.messages.create(
+        agent_id=agent.id,
+        messages=USER_MESSAGE_TEST_APPROVAL,
+    )
+    tool_call_id = response.messages[-1].tool_call.tool_call_id
+
+    client.agents.messages.create(
+        agent_id=agent.id,
+        messages=[
+            {
+                "type": "approval",
+                "approvals": [
+                    {
+                        "type": "approval",
+                        "approve": True,
+                        "tool_call_id": tool_call_id,
+                    },
+                ],
+            },
+            {
+                "type": "message",
+                "role": "user",
+                "content": "The secret code should not contain any special characters.",
+            },
+        ],
+    )
+
+    response = client.agents.messages.stream(
+        agent_id=agent.id,
+        messages=USER_MESSAGE_FOLLOW_UP,
+        stream_tokens=True,
+    )
+
+    messages = accumulate_chunks(response)
+
+    assert messages is not None
+    assert messages[0].message_type in ["reasoning_message", "assistant_message", "tool_call_message"]
+    assert messages[-2].message_type == "stop_reason"
+    assert messages[-1].message_type == "usage_statistics"
+
+
 # ------------------------------
 # Deny Test Cases
 # ------------------------------
@@ -800,6 +845,51 @@ def test_deny_and_follow_up_with_error(
     assert messages[-1].message_type == "usage_statistics"
 
 
+def test_deny_with_user_message(
+    client: Letta,
+    agent: AgentState,
+) -> None:
+    response = client.agents.messages.create(
+        agent_id=agent.id,
+        messages=USER_MESSAGE_TEST_APPROVAL,
+    )
+    tool_call_id = response.messages[-1].tool_call.tool_call_id
+
+    client.agents.messages.create(
+        agent_id=agent.id,
+        messages=[
+            {
+                "type": "approval",
+                "approvals": [
+                    {
+                        "type": "approval",
+                        "approve": False,
+                        "tool_call_id": tool_call_id,
+                    },
+                ],
+            },
+            {
+                "type": "message",
+                "role": "user",
+                "content": f"Actually, you don't need to call the tool, the secret code is {SECRET_CODE}",
+            },
+        ],
+    )
+
+    response = client.agents.messages.stream(
+        agent_id=agent.id,
+        messages=USER_MESSAGE_FOLLOW_UP,
+        stream_tokens=True,
+    )
+
+    messages = accumulate_chunks(response)
+
+    assert messages is not None
+    assert len(messages) > 2
+    assert messages[-2].message_type == "stop_reason"
+    assert messages[-1].message_type == "usage_statistics"
+
+
 # --------------------------------
 # Client-Side Execution Test Cases
 # --------------------------------
@@ -1020,6 +1110,52 @@ def test_client_side_tool_call_and_follow_up_with_error(
     assert messages[-1].message_type == "usage_statistics"
 
 
+def test_client_side_tool_call_with_user_message(
+    client: Letta,
+    agent: AgentState,
+) -> None:
+    response = client.agents.messages.create(
+        agent_id=agent.id,
+        messages=USER_MESSAGE_TEST_APPROVAL,
+    )
+    tool_call_id = response.messages[-1].tool_call.tool_call_id
+
+    client.agents.messages.create(
+        agent_id=agent.id,
+        messages=[
+            {
+                "type": "approval",
+                "approvals": [
+                    {
+                        "type": "tool",
+                        "tool_call_id": tool_call_id,
+                        "tool_return": SECRET_CODE,
+                        "status": "success",
+                    },
+                ],
+            },
+            {
+                "type": "message",
+                "role": "user",
+                "content": "The secret code should not contain any special characters.",
+            },
+        ],
+    )
+
+    response = client.agents.messages.stream(
+        agent_id=agent.id,
+        messages=USER_MESSAGE_FOLLOW_UP,
+        stream_tokens=True,
+    )
+
+    messages = accumulate_chunks(response)
+
+    assert messages is not None
+    assert len(messages) > 2
+    assert messages[-2].message_type == "stop_reason"
+    assert messages[-1].message_type == "usage_statistics"
+
+
 def test_parallel_tool_calling(
     client: Letta,
     agent: AgentState,