diff --git a/plinth/frontpage.py b/plinth/frontpage.py
index 171fb021d..5e63bff1c 100644
--- a/plinth/frontpage.py
+++ b/plinth/frontpage.py
@@ -5,7 +5,7 @@ Manage application shortcuts on front page.
 
 import json
 import logging
-import os
+import pathlib
 
 from plinth import app, cfg
 
@@ -129,8 +129,6 @@ class Shortcut(app.FollowerComponent):
 
 def add_custom_shortcuts():
     custom_shortcuts = get_custom_shortcuts()
-    if not custom_shortcuts:
-        return
 
     for shortcut in custom_shortcuts['shortcuts']:
         web_app_url = _extract_web_app_url(shortcut)
@@ -161,11 +159,20 @@ def _extract_web_app_url(custom_shortcut):
 
 
 def get_custom_shortcuts():
-    cfg_dir = os.path.dirname(cfg.config_file)
-    shortcuts_file = os.path.join(cfg_dir, 'custom-shortcuts.json')
-    if os.path.isfile(shortcuts_file) and os.stat(shortcuts_file).st_size:
-        logger.info('Loading custom shortcuts from %s', shortcuts_file)
-        with open(shortcuts_file) as shortcuts:
-            custom_shortcuts = json.load(shortcuts)
-            return custom_shortcuts
-    return None
+    """Return a merged dictionary of all custom shortcuts."""
+    shortcuts_dirs = [cfg.config_dir, cfg.data_dir, cfg.file_root]
+
+    shortcuts = {'shortcuts': []}
+    for shortcuts_dir in shortcuts_dirs:
+        file_path = pathlib.Path(shortcuts_dir) / 'custom-shortcuts.json'
+        if not file_path.is_file() or not file_path.stat().st_size:
+            continue
+
+        logger.info('Loading custom shortcuts from %s', file_path)
+        with file_path.open() as file_handle:
+            try:
+                shortcuts['shortcuts'] += json.load(file_handle)['shortcuts']
+            except (KeyError, json.JSONDecodeError):
+                logger.info('Error loading shortcuts from %s', file_path)
+
+    return shortcuts
diff --git a/plinth/modules/api/views.py b/plinth/modules/api/views.py
index 9fb5e82b9..d5a375409 100644
--- a/plinth/modules/api/views.py
+++ b/plinth/modules/api/views.py
@@ -40,9 +40,7 @@ def get_shortcuts_as_json(username=None):
         for shortcut in frontpage.Shortcut.list(username)
         if shortcut.component_id and shortcut.is_enabled()
     ]
-    custom_shortcuts = frontpage.get_custom_shortcuts()
-    if custom_shortcuts:
-        shortcuts += custom_shortcuts['shortcuts']
+    shortcuts += frontpage.get_custom_shortcuts()['shortcuts']
     return {'shortcuts': shortcuts}
 
 
diff --git a/plinth/tests/conftest.py b/plinth/tests/conftest.py
index 122dc1c11..2afad9b4a 100644
--- a/plinth/tests/conftest.py
+++ b/plinth/tests/conftest.py
@@ -31,7 +31,7 @@ NEXTCLOUD_SHORTCUT = {
 @pytest.fixture(name='custom_shortcuts_file')
 def fixture_custom_shortcuts_file(load_cfg, tmp_path):
     """Fixture to set path for a custom shortcuts file."""
-    load_cfg.config_file = str(tmp_path / 'plinth.conf')
+    load_cfg.config_dir = str(tmp_path)
     return tmp_path / 'custom-shortcuts.json'