diff --git a/.cirrus.yml b/.cirrus.yml
index 03c0904577..25201af5cb 100644
--- a/.cirrus.yml
+++ b/.cirrus.yml
@@ -374,7 +374,7 @@ bindings_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('pkg/bindings/test/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: &build
@@ -500,7 +500,7 @@ docker-py_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('test/python/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
@@ -527,7 +527,7 @@ unit_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('**/*_test.go') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
@@ -557,8 +557,8 @@ apiv2_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
-        changesInclude('test/apiv2/**') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('test/apiv2/**', 'test/python/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
     gce_instance: *standardvm
@@ -589,7 +589,7 @@ compose_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('test/compose/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
@@ -621,7 +621,7 @@ local_integration_test_task: &local_integration_test_task
     only_if: &only_if_int_test >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('test/e2e/**', 'test/utils/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
@@ -715,7 +715,7 @@ podman_machine_task:
     only_if: &only_if_machine_test >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('cmd/podman/machine/**', 'pkg/machine/**', '**/*machine*.go')
     depends_on: *build
     ec2_instance:
@@ -838,7 +838,7 @@ local_system_test_task: &local_system_test_task
     only_if: &only_if_system_test >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('test/system/**') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
@@ -930,7 +930,7 @@ farm_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('test/farm/**', 'test/system/*.bash') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
@@ -954,7 +954,7 @@ buildah_bud_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('**/*build*.go', 'test/buildah-bud/**')
     depends_on: *build
     env:
@@ -982,7 +982,7 @@ upgrade_test_task:
     only_if: >-
         $CIRRUS_PR == '' ||
         $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' ||
-        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') ||
+        changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf', 'hack/**', 'version/rawversion/*') ||
         changesInclude('test/upgrade/**', 'test/system/*.bash') ||
         (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))
     depends_on: *build
diff --git a/contrib/cirrus/cirrus_yaml_test.py b/contrib/cirrus/cirrus_yaml_test.py
index 49b1a41954..f127ffbfa2 100755
--- a/contrib/cirrus/cirrus_yaml_test.py
+++ b/contrib/cirrus/cirrus_yaml_test.py
@@ -62,7 +62,10 @@ class TestDependsOn(TestCaseBase):
 
     def test_only_if(self):
         """2024-07 PR#23174: ugly but necessary duplication in only_if conditions. Prevent typos or unwanted changes."""
-        beginning = "$CIRRUS_PR == '' || $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' || changesInclude('.cirrus.yml', 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'hack/**', 'version/rawversion/*') || "
+        # N/B: This giant string is white space sensitive, take care when updating/modifying
+        beginning = ("$CIRRUS_PR == '' || $CIRRUS_CHANGE_TITLE =~ '.*CI:ALL.*' || changesInclude('.cirrus.yml',"
+                     " 'Makefile', 'contrib/cirrus/**', 'vendor/**', 'test/tools/**', 'test/registries*.conf',"
+                     " 'hack/**', 'version/rawversion/*') || ")
         real_source_changes = " || (changesInclude('**/*.go', '**/*.c', '**/*.h') && !changesIncludeOnly('test/**', 'pkg/machine/e2e/**'))"
 
         for task_name in self.ALL_TASK_NAMES:
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)