diff --git a/pkg/reporegistry/error.go b/pkg/reporegistry/error.go
index 7e0938d7fe..34e7bb080b 100644
--- a/pkg/reporegistry/error.go
+++ b/pkg/reporegistry/error.go
@@ -1,13 +1,17 @@
 package reporegistry
 
-import "fmt"
+import (
+	"fmt"
+	"io/fs"
+)
 
 // NoReposLoadedError is an error type that is returned when no repositories
 // are loaded from the given paths.
 type NoReposLoadedError struct {
 	Paths []string
+	FSes  []fs.FS
 }
 
 func (e *NoReposLoadedError) Error() string {
-	return fmt.Sprintf("no repositories found in the given paths: %v", e.Paths)
+	return fmt.Sprintf("no repositories found in the given paths: %v/%v", e.Paths, e.FSes)
 }
diff --git a/pkg/reporegistry/reporegistry.go b/pkg/reporegistry/reporegistry.go
index 7a15e042ad..7e796fd028 100644
--- a/pkg/reporegistry/reporegistry.go
+++ b/pkg/reporegistry/reporegistry.go
@@ -2,6 +2,7 @@ package reporegistry
 
 import (
 	"fmt"
+	"io/fs"
 
 	"github.com/osbuild/images/pkg/distroidparser"
 	"github.com/osbuild/images/pkg/rpmmd"
@@ -14,10 +15,14 @@ type RepoRegistry struct {
 	repos rpmmd.DistrosRepoConfigs
 }
 
-// New returns a new RepoRegistry instance with the data
-// loaded from the given repoConfigPaths
-func New(repoConfigPaths []string) (*RepoRegistry, error) {
-	repositories, err := LoadAllRepositories(repoConfigPaths)
+// New returns a new RepoRegistry instance with the data loaded from
+// the given repoConfigPaths and repoConfigFS instance. The order is
+// important here, first the paths are tried, then the FSes.
+//
+// Note that the confPaths must point directly to the directory with
+// the json repo files.
+func New(repoConfigPaths []string, repoConfigFS []fs.FS) (*RepoRegistry, error) {
+	repositories, err := loadAllRepositories(repoConfigPaths, repoConfigFS)
 	if err != nil {
 		return nil, err
 	}
diff --git a/pkg/reporegistry/repository.go b/pkg/reporegistry/repository.go
index 4706724bef..47f239de8c 100644
--- a/pkg/reporegistry/repository.go
+++ b/pkg/reporegistry/repository.go
@@ -3,7 +3,6 @@ package reporegistry
 import (
 	"io/fs"
 	"os"
-	"path/filepath"
 	"strings"
 
 	"github.com/sirupsen/logrus"
@@ -12,23 +11,26 @@ import (
 	"github.com/osbuild/images/pkg/rpmmd"
 )
 
-// LoadAllRepositories loads all repositories for given distros from the given list of paths.
+// loadAllRepositories loads all repositories for given distros from the given list of paths.
 // Behavior is the same as with the LoadRepositories() method.
-func LoadAllRepositories(confPaths []string) (rpmmd.DistrosRepoConfigs, error) {
-	var confFSes []fs.FS
+func loadAllRepositories(confPaths []string, confFSes []fs.FS) (rpmmd.DistrosRepoConfigs, error) {
+	var mergedFSes []fs.FS
 
 	for _, confPath := range confPaths {
-		confFSes = append(confFSes, os.DirFS(filepath.Join(confPath, "repositories")))
+		mergedFSes = append(mergedFSes, os.DirFS(confPath))
+	}
+	for _, confFS := range confFSes {
+		mergedFSes = append(mergedFSes, confFS)
 	}
 
-	distrosRepoConfigs, err := LoadAllRepositoriesFromFS(confFSes)
+	distrosRepoConfigs, err := loadAllRepositoriesFromFS(mergedFSes)
 	if len(distrosRepoConfigs) == 0 {
-		return nil, &NoReposLoadedError{confPaths}
+		return nil, &NoReposLoadedError{confPaths, confFSes}
 	}
 	return distrosRepoConfigs, err
 }
 
-func LoadAllRepositoriesFromFS(confPaths []fs.FS) (rpmmd.DistrosRepoConfigs, error) {
+func loadAllRepositoriesFromFS(confPaths []fs.FS) (rpmmd.DistrosRepoConfigs, error) {
 	distrosRepoConfigs := rpmmd.DistrosRepoConfigs{}
 
 	for _, confPath := range confPaths {
@@ -89,9 +91,12 @@ func LoadAllRepositoriesFromFS(confPaths []fs.FS) (rpmmd.DistrosRepoConfigs, err
 // If there are duplicate distro repositories definitions found in multiple paths, the first
 // encounter is preferred. For this reason, the order of paths in the passed list should
 // reflect the desired preference.
+//
+// Note that the confPaths must point directly to the directory with
+// the json repo files.
 func LoadRepositories(confPaths []string, distro string) (map[string][]rpmmd.RepoConfig, error) {
 	var repoConfigs map[string][]rpmmd.RepoConfig
-	path := "/repositories/" + distro + ".json"
+	path := distro + ".json"
 
 	for _, confPath := range confPaths {
 		var err error
@@ -109,7 +114,7 @@ func LoadRepositories(confPaths []string, distro string) (map[string][]rpmmd.Rep
 	}
 
 	if repoConfigs == nil {
-		return nil, &NoReposLoadedError{confPaths}
+		return nil, &NoReposLoadedError{confPaths, nil}
 	}
 
 	return repoConfigs, nil
diff --git a/pkg/reporegistry/repository_test.go b/pkg/reporegistry/repository_test.go
index 0bcf75f63f..30a29b3951 100644
--- a/pkg/reporegistry/repository_test.go
+++ b/pkg/reporegistry/repository_test.go
@@ -19,8 +19,8 @@ import (
 
 func getConfPaths(t *testing.T) []string {
 	confPaths := []string{
-		"./test/confpaths/priority1",
-		"./test/confpaths/priority2",
+		"./test/confpaths/priority1/repositories",
+		"./test/confpaths/priority2/repositories",
 	}
 	var absConfPaths []string
 
@@ -280,7 +280,7 @@ func Test_LoadAllRepositories(t *testing.T) {
 
 	confPaths := getConfPaths(t)
 
-	distroReposMap, err := LoadAllRepositories(confPaths)
+	distroReposMap, err := loadAllRepositories(confPaths, nil)
 	assert.NotNil(t, distroReposMap)
 	assert.Nil(t, err)
 	assert.Equal(t, len(distroReposMap), len(expectedReposMap))
@@ -307,7 +307,7 @@ func TestLoadRepositoriesLogging(t *testing.T) {
 	logrus.AddHook(logHook)
 
 	confPaths := getConfPaths(t)
-	_, err := LoadAllRepositories(confPaths)
+	_, err := loadAllRepositories(confPaths, nil)
 	require.NoError(t, err)
 	needle := "Loaded repository configuration file: rhel-8.10.json"
 	assert.True(t, slices.ContainsFunc(logHook.AllEntries(), func(entry *logrus.Entry) bool {