diff --git a/fdroidserver/index.py b/fdroidserver/index.py
index ddb51546..d05d159e 100644
--- a/fdroidserver/index.py
+++ b/fdroidserver/index.py
@@ -711,6 +711,7 @@ def make_v2(apps, packages, repodir, repodict, requestsdict, fdroid_signing_key_
 
     output_packages = collections.OrderedDict()
     output['packages'] = output_packages
+    categories_used_by_apps = set()
     for package in packages:
         packageName = package['packageName']
         if packageName not in apps:
@@ -730,7 +731,9 @@ def make_v2(apps, packages, repodir, repodict, requestsdict, fdroid_signing_key_
         else:
             packagelist = {}
             output_packages[packageName] = packagelist
-            packagelist["metadata"] = package_metadata(apps[packageName], repodir)
+            app = apps[packageName]
+            categories_used_by_apps.update(app.get('Categories', []))
+            packagelist["metadata"] = package_metadata(app, repodir)
             if "signer" in package:
                 packagelist["metadata"]["preferredSigner"] = package["signer"]
 
@@ -738,6 +741,12 @@ def make_v2(apps, packages, repodir, repodict, requestsdict, fdroid_signing_key_
 
         packagelist["versions"][package["hash"]] = convert_version(package, apps[packageName], repodir)
 
+    if categories_used_by_apps and not output['repo'].get(CATEGORIES_CONFIG_NAME):
+        output['repo'][CATEGORIES_CONFIG_NAME] = dict()
+    for category in sorted(categories_used_by_apps):
+        if category not in output['repo'][CATEGORIES_CONFIG_NAME]:
+            output['repo'][CATEGORIES_CONFIG_NAME][category] = dict()
+
     entry = {}
     entry["timestamp"] = repodict["timestamp"]
 
diff --git a/tests/repo/entry.json b/tests/repo/entry.json
index 5c0ca528..0e8828e0 100644
--- a/tests/repo/entry.json
+++ b/tests/repo/entry.json
@@ -3,8 +3,8 @@
   "version": 20002,
   "index": {
     "name": "/index-v2.json",
-    "sha256": "7117ee6ff4ff2dd71ec3f3d3ad2ef7e9fd4afead9b1f2d39d0b224a1812e78b5",
-    "size": 53233,
+    "sha256": "b613858aa7a2ec476fcef5c841a5b8ff4b3b0f67f07678da981e2843f49c71ba",
+    "size": 53283,
     "numPackages": 10
   },
   "diffs": {}
diff --git a/tests/repo/index-v2.json b/tests/repo/index-v2.json
index 6ea92407..f45c1514 100644
--- a/tests/repo/index-v2.json
+++ b/tests/repo/index-v2.json
@@ -533,7 +533,10 @@
         "name": {
           "en-US": "System"
         }
-      }
+      },
+      "1": {},
+      "2.0": {},
+      "tests": {}
     },
     "requests": {
       "install": [
@@ -1443,4 +1446,4 @@
       }
     }
   }
-}
+}
\ No newline at end of file
diff --git a/tests/update.TestCase b/tests/update.TestCase
index 391dec93..e859e04f 100755
--- a/tests/update.TestCase
+++ b/tests/update.TestCase
@@ -53,6 +53,7 @@ import fdroidserver.common
 import fdroidserver.exception
 import fdroidserver.metadata
 import fdroidserver.update
+from fdroidserver.common import CATEGORIES_CONFIG_NAME
 
 
 DONATION_FIELDS = ('Donate', 'Liberapay', 'OpenCollective')
@@ -1804,6 +1805,99 @@ class UpdateTest(unittest.TestCase):
             fdroidserver.update.main()
         self.assertFalse(categories_txt.exists())
 
+    def test_no_blank_auto_defined_categories(self):
+        """When no app has Categories, there should be no definitions in the repo."""
+        os.chdir(self.testdir)
+        os.mkdir('metadata')
+        os.mkdir('repo')
+        Path('config.yml').write_text(
+            'repo_pubkey: ffffffffffffffffffffffffffffffffffffffff'
+        )
+
+        testapk = os.path.join('repo', 'com.politedroid_6.apk')
+        shutil.copy(os.path.join(self.basedir, testapk), testapk)
+        Path('metadata/com.politedroid.yml').write_text('Name: Polite')
+
+        with mock.patch('sys.argv', ['fdroid update', '--delete-unknown', '--nosign']):
+            fdroidserver.update.main()
+        with open('repo/index-v2.json') as fp:
+            index = json.load(fp)
+        self.assertFalse(CATEGORIES_CONFIG_NAME in index['repo'])
+
+    def test_auto_defined_categories(self):
+        """Repos that don't define categories in config/ should use auto-generated."""
+        os.chdir(self.testdir)
+        os.mkdir('metadata')
+        os.mkdir('repo')
+        Path('config.yml').write_text(
+            'repo_pubkey: ffffffffffffffffffffffffffffffffffffffff'
+        )
+
+        testapk = os.path.join('repo', 'com.politedroid_6.apk')
+        shutil.copy(os.path.join(self.basedir, testapk), testapk)
+        Path('metadata/com.politedroid.yml').write_text('Categories: [Time]')
+
+        with mock.patch('sys.argv', ['fdroid update', '--delete-unknown', '--nosign']):
+            fdroidserver.update.main()
+        with open('repo/index-v2.json') as fp:
+            index = json.load(fp)
+        self.assertEqual(
+            {'Time': dict()},
+            index['repo'][CATEGORIES_CONFIG_NAME],
+        )
+
+    def test_auto_defined_categories_two_apps(self):
+        """Repos that don't define categories in config/ should use auto-generated."""
+        os.chdir(self.testdir)
+        os.mkdir('metadata')
+        os.mkdir('repo')
+        Path('config.yml').write_text(
+            'repo_pubkey: ffffffffffffffffffffffffffffffffffffffff'
+        )
+
+        testapk = os.path.join('repo', 'com.politedroid_6.apk')
+        shutil.copy(os.path.join(self.basedir, testapk), testapk)
+        Path('metadata/com.politedroid.yml').write_text('Categories: [bar]')
+        testapk = os.path.join('repo', 'souch.smsbypass_9.apk')
+        shutil.copy(os.path.join(self.basedir, testapk), testapk)
+        Path('metadata/souch.smsbypass.yml').write_text('Categories: [foo, bar]')
+
+        with mock.patch('sys.argv', ['fdroid update', '--delete-unknown', '--nosign']):
+            fdroidserver.update.main()
+        with open('repo/index-v2.json') as fp:
+            index = json.load(fp)
+        self.assertEqual(
+            {'bar': dict(), 'foo': dict()},
+            index['repo'][CATEGORIES_CONFIG_NAME],
+        )
+
+    def test_auto_defined_categories_mix_into_config_categories(self):
+        """Repos that don't define all categories in config/ also use auto-generated."""
+        os.chdir(self.testdir)
+        os.mkdir('config')
+        Path('config/categories.yml').write_text('System: {name: System Apps}')
+        os.mkdir('metadata')
+        os.mkdir('repo')
+        Path('config.yml').write_text(
+            'repo_pubkey: ffffffffffffffffffffffffffffffffffffffff'
+        )
+
+        testapk = os.path.join('repo', 'com.politedroid_6.apk')
+        shutil.copy(os.path.join(self.basedir, testapk), testapk)
+        Path('metadata/com.politedroid.yml').write_text('Categories: [Time]')
+        testapk = os.path.join('repo', 'souch.smsbypass_9.apk')
+        shutil.copy(os.path.join(self.basedir, testapk), testapk)
+        Path('metadata/souch.smsbypass.yml').write_text('Categories: [System, Time]')
+
+        with mock.patch('sys.argv', ['fdroid update', '--delete-unknown', '--nosign']):
+            fdroidserver.update.main()
+        with open('repo/index-v2.json') as fp:
+            index = json.load(fp)
+        self.assertEqual(
+            {'System': {'name': {'en-US': 'System Apps'}}, 'Time': dict()},
+            index['repo'][CATEGORIES_CONFIG_NAME],
+        )
+
 
 if __name__ == "__main__":
     os.chdir(os.path.dirname(__file__))