diff --git a/frontend/src/core/islands/main.ts b/frontend/src/core/islands/main.ts
index ad750b12d63..25e8aaf61a0 100644
--- a/frontend/src/core/islands/main.ts
+++ b/frontend/src/core/islands/main.ts
@@ -202,6 +202,8 @@ export async function initialize() {
       case "model-lifecycle":
         handleWidgetMessage(MODEL_MANAGER, msg.data);
         return;
+      case "update-css":
+        return;
       default:
         logNever(msg.data);
     }
diff --git a/frontend/src/core/websocket/useMarimoKernelConnection.tsx b/frontend/src/core/websocket/useMarimoKernelConnection.tsx
index 92078b18f51..6f9a6a3ede0 100644
--- a/frontend/src/core/websocket/useMarimoKernelConnection.tsx
+++ b/frontend/src/core/websocket/useMarimoKernelConnection.tsx
@@ -304,6 +304,16 @@ export function useMarimoKernelConnection(opts: {
       case "update-cell-ids":
         setCellIds({ cellIds: msg.data.cell_ids as CellId[] });
         return;
+      case "update-css": {
+        let el = document.querySelector("style[title='marimo-custom']");
+        if (!el) {
+          el = document.createElement("style");
+          el.setAttribute("title", "marimo-custom");
+          document.head.append(el);
+        }
+        el.textContent = msg.data.css;
+        return;
+      }
       default:
         logNever(msg.data);
     }
diff --git a/marimo/_cli/development/commands.py b/marimo/_cli/development/commands.py
index 6baed3a6ce8..79ea57f82bb 100644
--- a/marimo/_cli/development/commands.py
+++ b/marimo/_cli/development/commands.py
@@ -133,6 +133,7 @@ def _generate_server_api_schema() -> dict[str, Any]:
         notifications.UpdateCellCodesNotification,
         notifications.UpdateCellIdsNotification,
         notifications.FocusCellNotification,
+        notifications.UpdateCssNotification,
         notifications.NotificationMessage,
         # ai
         ChatMessage,
diff --git a/marimo/_messaging/notification.py b/marimo/_messaging/notification.py
index 74e5860754b..34397d9bf20 100644
--- a/marimo/_messaging/notification.py
+++ b/marimo/_messaging/notification.py
@@ -731,6 +731,17 @@ class UpdateCellIdsNotification(Notification, tag="update-cell-ids"):
     cell_ids: list[CellId_t]
 
 
+class UpdateCssNotification(Notification, tag="update-css"):
+    """Pushes updated CSS content to the frontend.
+
+    Attributes:
+        css: The new CSS content (empty string clears custom CSS).
+    """
+
+    name: ClassVar[str] = "update-css"
+    css: str
+
+
 NotificationMessage = Union[
     # Cell operations
     CellNotification,
@@ -779,4 +790,6 @@ class UpdateCellIdsNotification(Notification, tag="update-cell-ids"):
     FocusCellNotification,
     UpdateCellCodesNotification,
     UpdateCellIdsNotification,
+    # CSS hot reload
+    UpdateCssNotification,
 ]
diff --git a/marimo/_server/api/endpoints/files.py b/marimo/_server/api/endpoints/files.py
index c75dbbb1c51..00b0f58bd3f 100644
--- a/marimo/_server/api/endpoints/files.py
+++ b/marimo/_server/api/endpoints/files.py
@@ -244,6 +244,32 @@ async def save_app_config(
     app_state = AppState(request)
     body = await parse_request(request, cls=SaveAppConfigurationRequest)
     session = app_state.require_current_session()
+
+    old_css_file = session.app_file_manager.app.config.css_file
     contents = session.app_file_manager.save_app_config(body.config)
 
+    # If css_file changed, push new CSS to the frontend and update watcher
+    if "css_file" in body.config:
+        new_css_file = session.app_file_manager.app.config.css_file
+        if old_css_file != new_css_file:
+            from marimo._messaging.notification import (
+                UpdateCssNotification,
+            )
+            from marimo._session.file_watcher_integration import (
+                SessionFileWatcherExtension,
+            )
+            from marimo._session.session import SessionImpl
+
+            css_content = session.app_file_manager.read_css_file() or ""
+            session.notify(
+                UpdateCssNotification(css=css_content),
+                from_consumer_id=None,
+            )
+
+            if isinstance(session, SessionImpl):
+                for ext in session.extensions:
+                    if isinstance(ext, SessionFileWatcherExtension):
+                        ext.update_css_watcher(session)
+                        break
+
     return PlainTextResponse(content=contents)
diff --git a/marimo/_session/file_watcher_integration.py b/marimo/_session/file_watcher_integration.py
index 917ec3678ab..d2e2cce6e02 100644
--- a/marimo/_session/file_watcher_integration.py
+++ b/marimo/_session/file_watcher_integration.py
@@ -11,6 +11,7 @@
 from typing import TYPE_CHECKING, Callable
 
 from marimo import _loggers
+from marimo._messaging.notification import UpdateCssNotification
 from marimo._session.events import (
     SessionEventBus,
     SessionEventListener,
@@ -26,6 +27,20 @@
     from collections.abc import Awaitable
 
 
+def _resolve_css_path(session: Session) -> Path | None:
+    """Resolve the absolute path to the CSS file from session config."""
+    css_file = session.app_file_manager.app.config.css_file
+    notebook_path = session.app_file_manager.path
+    if not css_file or not notebook_path:
+        return None
+
+    filepath = Path(css_file)
+    if not filepath.is_absolute():
+        filepath = Path(notebook_path).parent / filepath
+
+    return filepath
+
+
 class SessionFileWatcherExtension(SessionExtension, SessionEventListener):
     """Manages file watcher lifecycle for sessions."""
 
@@ -44,6 +59,7 @@ def __init__(
         self._event_bus: SessionEventBus | None = None
         self._session: Session | None = None
         self._on_change_callback = on_change_callback
+        self._css_path: Path | None = None
 
     def on_attach(self, session: Session, event_bus: SessionEventBus) -> None:
         """Attach the file watcher extension to a session."""
@@ -54,17 +70,59 @@ def on_attach(self, session: Session, event_bus: SessionEventBus) -> None:
         if not session.app_file_manager.path:
             return
 
-        # Register with the watcher manager
+        # Register notebook file watcher
         self._watcher_manager.add_callback(
             Path(session.app_file_manager.path), self._handle_file_change
         )
 
+        # Register CSS file watcher if configured
+        self._start_css_watcher(session)
+
         LOGGER.info(
             "Attached file watcher for session %s at path %s",
             session.initialization_id,
             session.app_file_manager.path,
         )
 
+    def _start_css_watcher(self, session: Session) -> None:
+        """Start watching the CSS file if configured."""
+        css_path = _resolve_css_path(session)
+        if css_path and css_path.exists():
+            self._css_path = css_path
+            self._watcher_manager.add_callback(
+                css_path, self._handle_css_change
+            )
+            LOGGER.debug("Watching CSS file: %s", css_path)
+
+    def _stop_css_watcher(self) -> None:
+        """Stop watching the current CSS file if any."""
+        if self._css_path:
+            self._watcher_manager.remove_callback(
+                self._css_path, self._handle_css_change
+            )
+            LOGGER.debug("Stopped watching CSS file: %s", self._css_path)
+            self._css_path = None
+
+    def update_css_watcher(self, session: Session) -> None:
+        """Update the CSS file watcher after a config change.
+
+        Compares the currently watched path with the new config and
+        registers/deregisters watchers as needed.
+        """
+        new_css_path = _resolve_css_path(session)
+
+        # Nothing changed
+        if self._css_path == new_css_path:
+            return
+
+        self._stop_css_watcher()
+        if new_css_path and new_css_path.exists():
+            self._css_path = new_css_path
+            self._watcher_manager.add_callback(
+                new_css_path, self._handle_css_change
+            )
+            LOGGER.debug("Updated CSS watcher to: %s", new_css_path)
+
     async def _handle_file_change(self, path: Path) -> None:
         """Handle a file change."""
         if not self._session:
@@ -72,6 +130,18 @@ async def _handle_file_change(self, path: Path) -> None:
 
         await self._on_change_callback(path, self._session)
 
+    async def _handle_css_change(self, path: Path) -> None:
+        """Handle a CSS file change by pushing new content to the frontend."""
+        if not self._session:
+            return
+
+        css_content = self._session.app_file_manager.read_css_file() or ""
+        self._session.notify(
+            UpdateCssNotification(css=css_content),
+            from_consumer_id=None,
+        )
+        LOGGER.debug("Sent CSS update for: %s", path)
+
     def on_detach(self) -> None:
         """Detach the file watcher extension from a session."""
         if not self._session:
@@ -80,12 +150,15 @@ def on_detach(self) -> None:
         if not self._session.app_file_manager.path:
             return
 
-        # Remove from watcher manager
+        # Remove notebook file watcher
         self._watcher_manager.remove_callback(
             self._canonicalize_path(self._session.app_file_manager.path),
             self._handle_file_change,
         )
 
+        # Remove CSS file watcher
+        self._stop_css_watcher()
+
         LOGGER.info(
             "Detached file watcher for session %s from path %s",
             self._session.initialization_id,
diff --git a/packages/openapi/api.yaml b/packages/openapi/api.yaml
index 26808828d31..01df54bead2 100644
--- a/packages/openapi/api.yaml
+++ b/packages/openapi/api.yaml
@@ -2453,6 +2453,7 @@ components:
           - $ref: '#/components/schemas/FocusCellNotification'
           - $ref: '#/components/schemas/UpdateCellCodesNotification'
           - $ref: '#/components/schemas/UpdateCellIdsNotification'
+          - $ref: '#/components/schemas/UpdateCssNotification'
           discriminator:
             mapping:
               alert: '#/components/schemas/AlertNotification'
@@ -2488,6 +2489,7 @@ components:
               storage-namespaces: '#/components/schemas/StorageNamespacesNotification'
               update-cell-codes: '#/components/schemas/UpdateCellCodesNotification'
               update-cell-ids: '#/components/schemas/UpdateCellIdsNotification'
+              update-css: '#/components/schemas/UpdateCssNotification'
               validate-sql-result: '#/components/schemas/ValidateSQLResultNotification'
               variable-values: '#/components/schemas/VariableValuesNotification'
               variables: '#/components/schemas/VariablesNotification'
@@ -4581,6 +4583,20 @@ components:
       - cellIdsToOutput
       title: UpdateCellOutputsRequest
       type: object
+    UpdateCssNotification:
+      description: "Pushes updated CSS content to the frontend.\n\n    Attributes:\n\
+        \        css: The new CSS content (empty string clears custom CSS)."
+      properties:
+        css:
+          type: string
+        op:
+          enum:
+          - update-css
+      required:
+      - op
+      - css
+      title: UpdateCssNotification
+      type: object
     UpdateUIElementCommand:
       description: "Update UI element values.\n\n    Triggered when users interact\
         \ with UI elements (sliders, inputs, dropdowns, etc.).\n    Updates element\
@@ -4938,7 +4954,7 @@ components:
       type: object
 info:
   title: marimo API
-  version: 0.19.10
+  version: 0.19.11
 openapi: 3.1.0
 paths:
   /@file/{filename_and_length}:
@@ -6311,3 +6327,4 @@ paths:
       summary: Submit login form
       tags:
       - auth
+
diff --git a/packages/openapi/src/api.ts b/packages/openapi/src/api.ts
index 867900cfbe5..563ea2a9e1b 100644
--- a/packages/openapi/src/api.ts
+++ b/packages/openapi/src/api.ts
@@ -4555,7 +4555,8 @@ export interface components {
         | components["schemas"]["CacheInfoNotification"]
         | components["schemas"]["FocusCellNotification"]
         | components["schemas"]["UpdateCellCodesNotification"]
-        | components["schemas"]["UpdateCellIdsNotification"];
+        | components["schemas"]["UpdateCellIdsNotification"]
+        | components["schemas"]["UpdateCssNotification"];
     };
     /**
      * LanguageServersConfig
@@ -5838,6 +5839,18 @@ export interface components {
         ];
       };
     };
+    /**
+     * UpdateCssNotification
+     * @description Pushes updated CSS content to the frontend.
+     *
+     *         Attributes:
+     *             css: The new CSS content (empty string clears custom CSS).
+     */
+    UpdateCssNotification: {
+      css: string;
+      /** @enum {unknown} */
+      op: "update-css";
+    };
     /**
      * UpdateUIElementCommand
      * @description Update UI element values.
diff --git a/tests/_session/test_file_watcher_integration.py b/tests/_session/test_file_watcher_integration.py
index 92ed94846ff..4611dbda978 100644
--- a/tests/_session/test_file_watcher_integration.py
+++ b/tests/_session/test_file_watcher_integration.py
@@ -17,11 +17,15 @@
 from marimo._utils.file_watcher import FileWatcherManager
 
 
-def create_mock_session(file_path: str | None):
+def create_mock_session(file_path: str | None, css_file: str | None = None):
     """Create a mock session for testing."""
     session = MagicMock()
     session.app_file_manager = MagicMock()
     session.app_file_manager.path = file_path
+    session.app_file_manager.app.config.css_file = css_file
+    session.app_file_manager.read_css_file.return_value = (
+        "body { color: red; }" if css_file else None
+    )
     return session
 
 
@@ -204,3 +208,167 @@ async def test_listener_on_session_closed_disabled(
 
     # Verify watcher was not detached
     watcher_manager.remove_callback.assert_not_called()
+
+
+def test_attach_with_css_file(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test that CSS file watcher is registered when css_file is configured."""
+    css_path = tmp_path / "custom.css"
+    css_path.write_text("body { color: red; }")
+    notebook_path = str(tmp_path / "notebook.py")
+
+    session = create_mock_session(notebook_path, css_file="custom.css")
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Should register both notebook and CSS watchers
+    assert watcher_manager.add_callback.call_count == 2
+    css_call = watcher_manager.add_callback.call_args_list[1]
+    assert css_call[0][0] == css_path
+
+
+def test_attach_without_css_file(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+) -> None:
+    """Test that no CSS watcher is registered when css_file is not set."""
+    session = create_mock_session("/path/to/notebook.py")
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Should only register the notebook watcher
+    assert watcher_manager.add_callback.call_count == 1
+
+
+def test_attach_css_file_does_not_exist(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test that no CSS watcher is registered when css_file doesn't exist."""
+    notebook_path = str(tmp_path / "notebook.py")
+    session = create_mock_session(notebook_path, css_file="missing.css")
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Should only register the notebook watcher
+    assert watcher_manager.add_callback.call_count == 1
+
+
+def test_detach_removes_css_watcher(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test that CSS watcher is cleaned up on detach."""
+    css_path = tmp_path / "custom.css"
+    css_path.write_text("body { color: red; }")
+    notebook_path = str(tmp_path / "notebook.py")
+
+    session = create_mock_session(notebook_path, css_file="custom.css")
+    lifecycle.on_attach(session, SessionEventBus())
+    lifecycle.on_detach()
+
+    # Should remove both notebook and CSS watchers
+    assert watcher_manager.remove_callback.call_count == 2
+
+
+async def test_css_change_sends_notification(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test that CSS file change sends UpdateCssNotification."""
+    from marimo._messaging.notification import UpdateCssNotification
+
+    css_path = tmp_path / "custom.css"
+    css_path.write_text("body { color: red; }")
+    notebook_path = str(tmp_path / "notebook.py")
+
+    session = create_mock_session(notebook_path, css_file="custom.css")
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Get the CSS callback (second add_callback call)
+    css_callback = watcher_manager.add_callback.call_args_list[1][0][1]
+
+    # Simulate CSS file change
+    await css_callback(css_path)
+
+    # Verify notification was sent
+    session.notify.assert_called_once()
+    notification = session.notify.call_args[0][0]
+    assert isinstance(notification, UpdateCssNotification)
+    assert notification.css == "body { color: red; }"
+
+
+def test_update_css_watcher_add(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test adding a CSS watcher mid-session."""
+    notebook_path = str(tmp_path / "notebook.py")
+    session = create_mock_session(notebook_path)
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Initially no CSS watcher
+    assert watcher_manager.add_callback.call_count == 1
+
+    # Now user sets css_file
+    css_path = tmp_path / "custom.css"
+    css_path.write_text("body { color: blue; }")
+    session.app_file_manager.app.config.css_file = "custom.css"
+
+    lifecycle.update_css_watcher(session)
+
+    # Should have registered the new CSS watcher
+    assert watcher_manager.add_callback.call_count == 2
+    css_call = watcher_manager.add_callback.call_args_list[1]
+    assert css_call[0][0] == css_path
+
+
+def test_update_css_watcher_remove(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test removing a CSS watcher mid-session."""
+    css_path = tmp_path / "custom.css"
+    css_path.write_text("body { color: red; }")
+    notebook_path = str(tmp_path / "notebook.py")
+
+    session = create_mock_session(notebook_path, css_file="custom.css")
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Now user clears css_file
+    session.app_file_manager.app.config.css_file = None
+
+    lifecycle.update_css_watcher(session)
+
+    # Should have removed the old CSS watcher
+    assert watcher_manager.remove_callback.call_count == 1
+
+
+def test_update_css_watcher_change(
+    lifecycle: SessionFileWatcherExtension,
+    watcher_manager: MagicMock,
+    tmp_path: Path,
+) -> None:
+    """Test changing from one CSS file to another mid-session."""
+    old_css = tmp_path / "old.css"
+    old_css.write_text("body { color: red; }")
+    new_css = tmp_path / "new.css"
+    new_css.write_text("body { color: blue; }")
+    notebook_path = str(tmp_path / "notebook.py")
+
+    session = create_mock_session(notebook_path, css_file="old.css")
+    lifecycle.on_attach(session, SessionEventBus())
+
+    # Change to new CSS file
+    session.app_file_manager.app.config.css_file = "new.css"
+    lifecycle.update_css_watcher(session)
+
+    # Should remove old and add new
+    assert watcher_manager.remove_callback.call_count == 1
+    # 2 from attach (notebook + old CSS) + 1 from update (new CSS)
+    assert watcher_manager.add_callback.call_count == 3