diff --git a/plinth/context_processors.py b/plinth/context_processors.py
index c1028758c..1518afa78 100644
--- a/plinth/context_processors.py
+++ b/plinth/context_processors.py
@@ -8,7 +8,7 @@ import re
 from django.utils.translation import gettext as _
 from django.utils.translation import gettext_noop
 
-from plinth import cfg
+from plinth import cfg, web_server
 from plinth.utils import is_user_admin
 
 
@@ -35,6 +35,7 @@ def common(request):
         'active_menu_urls': active_menu_urls,
         'box_name': _(cfg.box_name),
         'user_is_admin': is_user_admin(request, True),
+        'user_css': web_server.get_user_css(),
         'notifications': notifications_context['notifications'],
         'notifications_max_severity': notifications_context['max_severity']
     }
diff --git a/plinth/templates/base.html b/plinth/templates/base.html
index e3897abb4..c2f5c6215 100644
--- a/plinth/templates/base.html
+++ b/plinth/templates/base.html
@@ -50,10 +50,14 @@
   <link rel="apple-touch-icon" sizes="72x72" href="{% static 'theme/img/apple-touch-icon-72px-precomposed.png' %}"/>
   <link rel="apple-touch-icon" sizes="114x114" href="{% static 'theme/img/apple-touch-icon-114px-precomposed.png' %}"/>
 
-  <!-- Bootstrap base CSS -->
+  <!-- Stylesheets -->
   <link rel="stylesheet" href="{% static '/javascript/bootstrap4/css/bootstrap.min.css' %}"/>
   <link rel="stylesheet" href="{% static '/javascript/fork-awesome/css/fork-awesome.css' %}"/>
   <link rel="stylesheet" href="{% static 'theme/css/main.css' %}"/>
+  {% if user_css %}
+    <link rel="stylesheet" href="{% static user_css %}"/>
+  {% endif %}
+
   <!-- Local link to system jQuery -->
   <!-- TODO Deferring jQuery is causing scripts to be loaded before jQuery is available -->
   <script type="text/javascript" src="{% static '/javascript/jquery/jquery.min.js' %}"></script>
diff --git a/plinth/web_server.py b/plinth/web_server.py
index 6b6317598..9020c8be4 100644
--- a/plinth/web_server.py
+++ b/plinth/web_server.py
@@ -5,6 +5,7 @@ Setup CherryPy web server.
 
 import logging
 import os
+import pathlib
 import sys
 import warnings
 from typing import ClassVar
@@ -27,6 +28,24 @@ MODULES_EXCLUDED_FROM_AUTORELOAD = [
     'psycopg2',
 ]
 
+_CUSTOM_STATIC_URL = '/custom/static'
+
+_USER_CSS_PATH = 'css/user.css'
+
+
+def get_custom_static_url():
+    """Return the URL path fragment for custom static URL."""
+    return f'{cfg.server_dir}{_CUSTOM_STATIC_URL}'
+
+
+def get_user_css():
+    """Return the URL path fragement for user CSS if it exists else None."""
+    user_css_path = pathlib.Path(cfg.custom_static_dir) / _USER_CSS_PATH
+    if not user_css_path.exists():
+        return None
+
+    return get_custom_static_url() + '/' + _USER_CSS_PATH
+
 
 def _mount_static_directory(static_dir, static_url):
     config = {
@@ -64,7 +83,7 @@ def init():
     _mount_static_directory(static_dir, web_framework.get_static_url())
 
     custom_static_dir = cfg.custom_static_dir
-    custom_static_url = '/plinth/custom/static'
+    custom_static_url = get_custom_static_url()
     if os.path.exists(custom_static_dir):
         _mount_static_directory(custom_static_dir, custom_static_url)
     else: