diff --git a/tests/functional/flakes/flake-registry.sh b/tests/functional/flakes/flake-registry.sh
deleted file mode 100644
index 5e72bd05a..000000000
--- a/tests/functional/flakes/flake-registry.sh
+++ /dev/null
@@ -1,73 +0,0 @@
-source ./common.sh
-
-# remove the flake registry from nix.conf, to set to default ("vendored")
-sed -i '/flake-registry/d' "$NIX_CONF_DIR/nix.conf"
-
-# Make sure the vendored registry contains the correct amount.
-[[ $(nix registry list | wc -l) == 37 ]]
-# sanity check, contains the important ones
-nix registry list | grep '^global flake:nixpkgs'
-nix registry list | grep '^global flake:home-manager'
-
-
-# it should work the same if we set to vendored directly.
-echo 'flake-registry = vendored' >> "$NIX_CONF_DIR/nix.conf"
-[[ $(nix registry list | wc -l) == 37 ]]
-# sanity check, contains the important ones
-nix registry list | grep '^global flake:nixpkgs'
-nix registry list | grep '^global flake:home-manager'
-
-
-# the online flake registry should still work, but it is deprecated.
-set -m
-# port 0: auto pick a free port, unbufferred output
-python3 -u -m http.server 0 --bind 127.0.0.1 > server.out &
-
-# wait for the http server to admit it is working
-while ! grep -qP 'port \d+' server.out ; do
-  echo 'waiting for python http' >&2
-  sleep 0.2
-done
-
-port=$(awk 'match($0,/port ([[:digit:]]+)/, ary) { print ary[1] }' server.out)
-
-sed -i '/flake-registry/d' "$NIX_CONF_DIR/nix.conf"
-echo "flake-registry = http://127.0.0.1:$port/flake-registry.json" >> "$NIX_CONF_DIR/nix.conf"
-cat <<EOF > flake-registry.json
-{
-    "flakes": [
-        {
-        "from": {
-            "type": "indirect",
-            "id": "nixpkgs"
-        },
-        "to": {
-            "type": "github",
-            "owner": "NixOS",
-            "repo": "nixpkgs"
-        }
-        },
-        {
-        "from": {
-            "type": "indirect",
-            "id": "private-flake"
-        },
-        "to": {
-            "type": "github",
-            "owner": "fancy-enterprise",
-            "repo": "private-flake"
-        }
-        }
-    ],
-    "version": 2
-}
-EOF
-
-[[ $(nix registry list | wc -l) == 2 ]]
-nix registry list | grep '^global flake:nixpkgs'
-nix registry list | grep '^global flake:private-flake'
-
-# make sure we have a warning:
-nix registry list 2>&1 | grep "config option flake-registry referring to a URL is deprecated and will be removed"
-
-kill %python
diff --git a/tests/functional/meson.build b/tests/functional/meson.build
index 7ce6a9a8c..23b1d55be 100644
--- a/tests/functional/meson.build
+++ b/tests/functional/meson.build
@@ -38,7 +38,6 @@ functional_tests_scripts = [
   'flakes/mercurial.sh',
   'flakes/follow-paths.sh',
   'flakes/flake-in-submodule.sh',
-  'flakes/flake-registry.sh',
   'gc.sh',
   'nix-collect-garbage-d.sh',
   'nix-collect-garbage-dry-run.sh',
diff --git a/tests/functional2/flakes/test_registry.py b/tests/functional2/flakes/test_registry.py
new file mode 100644
index 000000000..96c4a13d1
--- /dev/null
+++ b/tests/functional2/flakes/test_registry.py
@@ -0,0 +1,55 @@
+from testlib.fixtures.nix import Nix
+import aiohttp.web as web
+from testlib.fixtures.http_server import http_server
+import pytest
+import json
+
+
+@pytest.mark.parametrize("registry", [None, "vendored"])
+def test_default_registry(nix: Nix, registry: str | None):
+    nix.settings.flake_registry = registry
+    items = nix.nix(["registry", "list"], flake=True).run().ok().stdout_s.splitlines()
+    # Make sure the vendored registry contains the correct amount.
+    assert len(items) == 37
+    # sanity check, contains the important ones
+    assert any(item.startswith("global flake:nixpkgs") for item in items)
+    assert any(item.startswith("global flake:home-manager") for item in items)
+
+
+online_registry = {
+    "flakes": [
+        {
+            "from": {"type": "indirect", "id": "nixpkgs"},
+            "to": {"type": "github", "owner": "NixOS", "repo": "nixpkgs"},
+        },
+        {
+            "from": {"type": "indirect", "id": "private-flake"},
+            "to": {"type": "github", "owner": "fancy-enterprise", "repo": "private-flake"},
+        },
+    ],
+    "version": 2,
+}
+
+
+class TestOnlineRegistry:
+    async def get_registry(self, _req: web.Request) -> web.Response:
+        return web.Response(text=json.dumps(online_registry))
+
+    def test_online_registry(self, nix: Nix):
+        app = web.Application()
+        app.add_routes([web.get("/flake-registry.json", self.get_registry)])
+
+        with http_server(app) as httpd:
+            nix.settings.flake_registry = f"http://localhost:{httpd.port}/flake-registry.json"
+
+            result = nix.nix(["registry", "list"], flake=True).run().ok()
+            assert result.stdout_s.splitlines() == [
+                "global flake:nixpkgs github:NixOS/nixpkgs",
+                "global flake:private-flake github:fancy-enterprise/private-flake",
+            ]
+
+            # make sure there's a warning
+            assert (
+                "config option flake-registry referring to a URL is deprecated and will be removed"
+                in result.stderr_s
+            )