diff --git a/.gitignore b/.gitignore
index cc79f847eb..f2272e91eb 100644
--- a/.gitignore
+++ b/.gitignore
@@ -40,6 +40,7 @@ pnpm-debug.log*
 lerna-debug.log*
 
 node_modules
+.pnpm-store
 dist
 dist-ssr
 *.local
@@ -61,4 +62,4 @@ dist-ssr
 backend/README.md
 backend/.dmypy.json
 
-.history
\ No newline at end of file
+.history
diff --git a/backend/chainlit/server.py b/backend/chainlit/server.py
index c281cff124..035dc6ccc3 100644
--- a/backend/chainlit/server.py
+++ b/backend/chainlit/server.py
@@ -147,6 +147,14 @@ async def watch_files_for_changes():
 
         discord_task = asyncio.create_task(client.start(discord_bot_token))
 
+    slack_task = None
+
+    # Slack Socket Handler if env variable SLACK_WEBSOCKET_TOKEN is set
+    if os.environ.get("SLACK_BOT_TOKEN") and os.environ.get("SLACK_WEBSOCKET_TOKEN"):
+        from chainlit.slack.app import start_socket_mode
+
+        slack_task = asyncio.create_task(start_socket_mode())
+
     try:
         yield
     finally:
@@ -162,6 +170,10 @@ async def watch_files_for_changes():
             if discord_task:
                 discord_task.cancel()
                 await discord_task
+
+            if slack_task:
+                slack_task.cancel()
+                await slack_task
         except asyncio.exceptions.CancelledError:
             pass
 
@@ -294,10 +306,14 @@ async def serve_copilot_file(
 
 
 # -------------------------------------------------------------------------------
-#                               SLACK HANDLER
+#                               SLACK HTTP HANDLER
 # -------------------------------------------------------------------------------
 
-if os.environ.get("SLACK_BOT_TOKEN") and os.environ.get("SLACK_SIGNING_SECRET"):
+if (
+    os.environ.get("SLACK_BOT_TOKEN")
+    and os.environ.get("SLACK_SIGNING_SECRET")
+    and not os.environ.get("SLACK_WEBSOCKET_TOKEN")
+):
     from chainlit.slack.app import slack_app_handler
 
     @router.post("/slack/events")
diff --git a/backend/chainlit/slack/app.py b/backend/chainlit/slack/app.py
index 332a0f9283..f592284785 100644
--- a/backend/chainlit/slack/app.py
+++ b/backend/chainlit/slack/app.py
@@ -7,6 +7,7 @@
 
 import httpx
 from slack_bolt.adapter.fastapi.async_handler import AsyncSlackRequestHandler
+from slack_bolt.adapter.socket_mode.async_handler import AsyncSocketModeHandler
 from slack_bolt.async_app import AsyncApp
 
 from chainlit.config import config
@@ -125,6 +126,16 @@ async def update_step(self, step_dict: StepDict):
 )
 
 
+async def start_socket_mode():
+    """
+    Initializes and starts the Slack app in Socket Mode asynchronously.
+
+    Uses the SLACK_WEBSOCKET_TOKEN from environment variables to authenticate.
+    """
+    handler = AsyncSocketModeHandler(slack_app, os.environ.get("SLACK_WEBSOCKET_TOKEN"))
+    await handler.start_async()
+
+
 def init_slack_context(
     session: HTTPSession,
     slack_channel_id: str,
diff --git a/backend/tests/test_slack_socket_mode.py b/backend/tests/test_slack_socket_mode.py
new file mode 100644
index 0000000000..8e0e4368a4
--- /dev/null
+++ b/backend/tests/test_slack_socket_mode.py
@@ -0,0 +1,54 @@
+# tests/test_slack_socket_mode.py
+import importlib
+from unittest.mock import AsyncMock, patch
+
+import pytest
+
+
+@pytest.mark.asyncio
+async def test_start_socket_mode_starts_handler(monkeypatch):
+    """
+    The function should:
+      • build an AsyncSocketModeHandler with the global slack_app
+      • use the token found in SLACK_WEBSOCKET_TOKEN
+      • await the handler.start_async() coroutine exactly once
+    """
+    token = "xapp-fake-token"
+    # minimal env required for the Slack module to initialise
+    monkeypatch.setenv("SLACK_BOT_TOKEN", "xoxb-fake-bot")
+    monkeypatch.setenv("SLACK_WEBSOCKET_TOKEN", token)
+
+    # Import the module first to avoid lazy import registry issues
+    slack_app_mod = importlib.import_module("chainlit.slack.app")
+
+    # Patch the object directly instead of using string path
+    with patch.object(
+        slack_app_mod, "AsyncSocketModeHandler", autospec=True
+    ) as handler_cls:
+        handler_instance = AsyncMock()
+        handler_cls.return_value = handler_instance
+
+        # Run: should build handler + await start_async
+        await slack_app_mod.start_socket_mode()
+
+        handler_cls.assert_called_once_with(slack_app_mod.slack_app, token)
+        handler_instance.start_async.assert_awaited_once()
+
+
+def test_slack_http_route_registered(monkeypatch):
+    """
+    When only the classic HTTP tokens are set (no websocket token),
+    the FastAPI app should expose POST /slack/events.
+    """
+    # HTTP-only environment
+    monkeypatch.setenv("SLACK_BOT_TOKEN", "xoxb-fake-bot")
+    monkeypatch.setenv("SLACK_SIGNING_SECRET", "shhh-fake-secret")
+    monkeypatch.delenv("SLACK_WEBSOCKET_TOKEN", raising=False)
+
+    # Re-import server with the fresh env so the route table is built correctly
+    server = importlib.reload(importlib.import_module("chainlit.server"))
+
+    assert any(
+        route.path == "/slack/events" and "POST" in route.methods
+        for route in server.router.routes
+    ), "Slack HTTP handler route was not registered"