diff --git a/tests/gateway/test_compress_command.py b/tests/gateway/test_compress_command.py
index 4cf51429cac9..708076543f2e 100644
--- a/tests/gateway/test_compress_command.py
+++ b/tests/gateway/test_compress_command.py
@@ -90,6 +90,48 @@ async def test_compress_command_reports_noop_without_success_banner():
     agent_instance.close.assert_called_once()
 
 
+@pytest.mark.asyncio
+async def test_compress_command_works_when_auto_compaction_disabled():
+    """compression.enabled: false disables *automatic* compaction only.
+
+    The gateway /compress handler has never gated on the flag — pin that
+    contract (every manual-compress surface must allow manual compression
+    regardless of the auto toggle, #64438) and the force=True cooldown
+    bypass that manual compression relies on."""
+    history = _make_history()
+    compressed = [
+        history[0],
+        {"role": "assistant", "content": "compressed summary"},
+        history[-1],
+    ]
+    runner = _make_runner(history)
+    agent_instance = MagicMock()
+    agent_instance.shutdown_memory_provider = MagicMock()
+    agent_instance.close = MagicMock()
+    agent_instance._cached_system_prompt = ""
+    agent_instance.tools = None
+    agent_instance.compression_enabled = False
+    agent_instance.context_compressor.has_content_to_compress.return_value = True
+    agent_instance.session_id = "sess-1"
+    agent_instance._compress_context.return_value = (compressed, "")
+
+    def _estimate(messages, **_kwargs):
+        return 100 if messages == history else 60
+
+    with (
+        patch("gateway.run._resolve_runtime_agent_kwargs", return_value={"api_key": "test-key"}),
+        patch("gateway.run._resolve_gateway_model", return_value="test-model"),
+        patch("run_agent.AIAgent", return_value=agent_instance),
+        patch("agent.model_metadata.estimate_request_tokens_rough", side_effect=_estimate),
+    ):
+        result = await runner._handle_compress_command(_make_event())
+
+    assert "disabled" not in result.lower()
+    assert "Compressed:" in result
+    agent_instance._compress_context.assert_called_once()
+    assert agent_instance._compress_context.call_args.kwargs.get("force") is True
+
+
 @pytest.mark.asyncio
 async def test_compress_command_explains_when_token_estimate_rises():
     history = _make_history()
diff --git a/tests/test_tui_gateway_server.py b/tests/test_tui_gateway_server.py
index 5eadd319731f..baeb4101c9c4 100644
--- a/tests/test_tui_gateway_server.py
+++ b/tests/test_tui_gateway_server.py
@@ -5892,6 +5892,37 @@ def test_compress_session_history_passes_force():
     assert agent._compress_context.call_args.kwargs.get("force") is True
 
 
+def test_compress_session_history_works_when_auto_compaction_disabled():
+    """compression.enabled: false disables *automatic* compaction only —
+    manual /compress must still work on every TUI route (session.compress
+    RPC, slash compress/compact, slash-worker mirror), all of which converge
+    on _compress_session_history. Pin that the helper never gates on
+    agent.compression_enabled (#64438)."""
+    from unittest.mock import MagicMock
+
+    agent = MagicMock()
+    agent.compression_enabled = False
+    agent.context_compressor = None  # keep _get_usage on the simple path
+    compressed = [{"role": "user", "content": "summary"}]
+    agent._compress_context.return_value = (compressed, "")
+    session = _session(
+        agent=agent,
+        history=[
+            {"role": "user", "content": "one"},
+            {"role": "assistant", "content": "two"},
+            {"role": "user", "content": "three"},
+            {"role": "assistant", "content": "four"},
+        ],
+    )
+
+    removed, _usage = server._compress_session_history(session)
+
+    assert removed == 3
+    assert session["history"] == compressed
+    agent._compress_context.assert_called_once()
+    assert agent._compress_context.call_args.kwargs.get("force") is True
+
+
 def test_session_compress_uses_compress_helper(monkeypatch):
     agent = types.SimpleNamespace()
     server._sessions["sid"] = _session(agent=agent)