diff --git a/gateway/run.py b/gateway/run.py
index 08f6b374485a4..3a890176c0abc 100644
--- a/gateway/run.py
+++ b/gateway/run.py
@@ -13518,7 +13518,7 @@ class GatewayRunner(GatewayAuthorizationMixin, GatewayKanbanWatchersMixin, Gatew
                     channel_prompt=event.channel_prompt,
                     channel_context=event.channel_context,
                 )
-                adapter._pending_messages[quick_key] = queued_event
+                self._enqueue_fifo(quick_key, queued_event, adapter)
             return "Agent still starting — /steer queued for the next turn."
         if running_agent and hasattr(running_agent, "steer"):
             try:
@@ -13541,7 +13541,7 @@ class GatewayRunner(GatewayAuthorizationMixin, GatewayKanbanWatchersMixin, Gatew
                 channel_prompt=event.channel_prompt,
                 channel_context=event.channel_context,
             )
-            adapter._pending_messages[quick_key] = queued_event
+            self._enqueue_fifo(quick_key, queued_event, adapter)
         return "No active agent — /steer queued for the next turn."
 
     async def _busy_goal_command(self, event: MessageEvent, quick_key: str, source):
diff --git a/tests/gateway/test_steer_fifo_overwrite.py b/tests/gateway/test_steer_fifo_overwrite.py
new file mode 100644
index 0000000000000..e3bffe5cb869b
--- /dev/null
+++ b/tests/gateway/test_steer_fifo_overwrite.py
@@ -0,0 +1,97 @@
+"""Regression tests for #75164 — /steer fallback must not overwrite FIFO head.
+
+Uses the real gateway test fixtures (tests/gateway/test_steer_command.py) to
+exercise both /steer fallback paths through _handle_message, proving that a
+pre-queued Q1/Q2 survives a /steer Q3 dispatch.
+
+Covers:
+- pending-sentinel path (agent not booted yet) -> _enqueue_fifo preserves Q1
+- no-steer() path (agent lacks steer()) -> _enqueue_fifo preserves Q1
+"""
+from __future__ import annotations
+
+import pytest
+
+from gateway.run import _AGENT_PENDING_SENTINEL
+from tests.gateway.test_steer_command import (
+    _make_event,
+    _make_runner,
+    _session_entry,
+    _make_source,
+)
+from gateway.session import build_session_key
+from unittest.mock import MagicMock
+
+
+def _prequeue(runner, adapter, sk):
+    """Pre-stage Q1 in the pending slot and Q2 in the overflow tail."""
+    from gateway.platforms.base import MessageEvent, MessageType
+
+    # Ensure _queued_events is initialized (mirrors GatewayRunner.__init__)
+    if not hasattr(runner, "_queued_events"):
+        runner._queued_events = {}
+
+    q1 = MessageEvent(
+        text="Q1",
+        source=_make_source(),
+        message_id="m1",
+        channel_context="ctx1",
+        message_type=MessageType.TEXT,
+    )
+    q2 = MessageEvent(
+        text="Q2",
+        source=_make_source(),
+        message_id="m2",
+        channel_context="ctx2",
+        message_type=MessageType.TEXT,
+    )
+    # Q1 -> pending slot (head), Q2 -> overflow tail
+    runner._enqueue_fifo(sk, q1, adapter)
+    runner._enqueue_fifo(sk, q2, adapter)
+    assert adapter._pending_messages[sk].text == "Q1"
+    assert runner._queued_events[sk][0].text == "Q2"
+
+
+@pytest.mark.asyncio
+async def test_steer_pending_sentinel_preserves_fifo_head():
+    """Issue #75164: /steer Q3 must not overwrite pre-queued Q1."""
+    runner, adapter = _make_runner(_session_entry())
+    sk = build_session_key(_make_source())
+    runner._running_agents[sk] = _AGENT_PENDING_SENTINEL
+
+    _prequeue(runner, adapter, sk)
+
+    result = await runner._handle_message(
+        _make_event("/steer wait up", channel_context="ctx3")
+    )
+    assert result is not None
+    assert "queued" in result.lower()
+
+    # Q1 still in slot, Q2 in overflow, Q3 appended to overflow — order preserved
+    assert adapter._pending_messages[sk].text == "Q1"
+    overflow = runner._queued_events[sk]
+    texts = [msg.text for msg in overflow]
+    assert texts == ["Q2", "wait up"], f"FIFO order broken: {texts}"
+
+
+@pytest.mark.asyncio
+async def test_steer_no_steer_method_preserves_fifo_head():
+    """Issue #75164: no-steer() fallback must not overwrite pre-queued Q1."""
+    runner, adapter = _make_runner(_session_entry())
+    sk = build_session_key(_make_source())
+
+    # Bare mock with NO steer() method
+    runner._running_agents[sk] = MagicMock(spec=[])
+
+    _prequeue(runner, adapter, sk)
+
+    result = await runner._handle_message(
+        _make_event("/steer fallback", channel_context="ctx3")
+    )
+    assert result is not None
+    assert "queued" in result.lower()
+
+    assert adapter._pending_messages[sk].text == "Q1"
+    overflow = runner._queued_events[sk]
+    texts = [msg.text for msg in overflow]
+    assert texts == ["Q2", "fallback"], f"FIFO order broken: {texts}"