diff --git a/.cirrus.yml b/.cirrus.yml
index cb45ef9d72..25201af5cb 100644
--- a/.cirrus.yml
+++ b/.cirrus.yml
@@ -558,7 +558,7 @@ apiv2_test_task:
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
         changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
-        changesInclude('test/apiv2/**') ||
+        changesInclude('test/apiv2/**', 'test/python/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
     gce_instance: *standardvm
diff --git a/test/python/docker/__init__.py b/test/python/docker/__init__.py
index d46f465f79..78ff5c3725 100644
--- a/test/python/docker/__init__.py
+++ b/test/python/docker/__init__.py
@@ -44,17 +44,27 @@ class PodmanAPI:
         os.environ["CONTAINERS_REGISTRIES_CONF"] = os.path.join(
             self.anchor_directory, "registry.conf"
         )
-        conf = """unqualified-search-registries = ["docker.io", "quay.io"]
 
-[[registry]]
-location="localhost:5000"
-insecure=true
+        # Entry verified by compat/test_system.py
+        reg_conf_sfx = """
 
 [[registry.mirror]]
 location = "mirror.localhost:5000"
 
 """
 
+        # Assume developer-mode testing by default
+        reg_conf_source_path="./test/registries.conf"
+
+        # When operating in a CI environment, use the local registry server.
+        # Ref: https://github.com/containers/automation_images/pull/357
+        #      https://github.com/containers/podman/pull/22726
+        if os.getenv("CI_USE_REGISTRY_CACHE"):
+            reg_conf_source_path = "./test/registries-cached.conf"
+
+        with open(os.path.join(reg_conf_source_path)) as file:
+            conf = file.read() + reg_conf_sfx
+
         with open(os.environ["CONTAINERS_REGISTRIES_CONF"], "w") as file:
             file.write(conf)