diff --git a/pkg/handlers/generic/mutation/mirrors/mirror.go b/pkg/handlers/generic/mutation/mirrors/mirror.go
index 17a62b5ea..27e5e46da 100644
--- a/pkg/handlers/generic/mutation/mirrors/mirror.go
+++ b/pkg/handlers/generic/mutation/mirrors/mirror.go
@@ -8,6 +8,8 @@ import (
 	"context"
 	_ "embed"
 	"fmt"
+	"net/url"
+	"path"
 	"text/template"
 
 	corev1 "k8s.io/api/core/v1"
@@ -97,11 +99,15 @@ func generateGlobalRegistryMirrorFile(mirror *mirrorConfig) ([]cabpkv1.File, err
 	if mirror == nil {
 		return nil, nil
 	}
+	formattedURL, err := formatURLForContainerd(mirror.URL)
+	if err != nil {
+		return nil, fmt.Errorf("failed formatting registry mirror URL for Containerd: %w", err)
+	}
 	templateInput := struct {
 		URL        string
 		CACertPath string
 	}{
-		URL: mirror.URL,
+		URL: formattedURL,
 	}
 	// CA cert is optional for mirror registry.
 	// i.e. registry is using signed certificates. Insecure registry will not be allowed.
@@ -110,7 +116,7 @@ func generateGlobalRegistryMirrorFile(mirror *mirrorConfig) ([]cabpkv1.File, err
 	}
 
 	var b bytes.Buffer
-	err := defaultRegistryMirrorPatchTemplate.Execute(&b, templateInput)
+	err = defaultRegistryMirrorPatchTemplate.Execute(&b, templateInput)
 	if err != nil {
 		return nil, fmt.Errorf("failed executing template for registry mirror: %w", err)
 	}
@@ -143,3 +149,20 @@ func generateMirrorCACertFile(
 		},
 	}
 }
+
+func formatURLForContainerd(uri string) (string, error) {
+	mirrorURL, err := url.ParseRequestURI(uri)
+	if err != nil {
+		return "", fmt.Errorf("failed parsing mirror: %w", err)
+	}
+
+	mirror := fmt.Sprintf("%s://%s", mirrorURL.Scheme, mirrorURL.Host)
+	// assume Containerd expects the following pattern:
+	//   scheme://host/v2/path
+	mirrorPath := "v2"
+	if mirrorURL.Path != "" {
+		mirrorPath = path.Join(mirrorPath, mirrorURL.Path)
+	}
+	// using path.Join on all elements incorrectly drops a "/" from "https://"
+	return fmt.Sprintf("%s/%s", mirror, mirrorPath), nil
+}
diff --git a/pkg/handlers/generic/mutation/mirrors/mirror_test.go b/pkg/handlers/generic/mutation/mirrors/mirror_test.go
index 8a16bea61..cdc7fdeec 100644
--- a/pkg/handlers/generic/mutation/mirrors/mirror_test.go
+++ b/pkg/handlers/generic/mutation/mirrors/mirror_test.go
@@ -31,8 +31,31 @@ func Test_generateDefaultRegistryMirrorFile(t *testing.T) {
 					Permissions: "0600",
 					Encoding:    "",
 					Append:      false,
-					Content: `[host."https://123456789.dkr.ecr.us-east-1.amazonaws.com"]
+					Content: `[host."https://123456789.dkr.ecr.us-east-1.amazonaws.com/v2"]
   capabilities = ["pull", "resolve"]
+  # don't rely on Containerd to add the v2/ suffix
+  # there is a bug where it is added incorrectly for mirrors with a path
+  override_path = true
+`,
+				},
+			},
+			wantErr: nil,
+		},
+		{
+			name:   "ECR image registry with a path and no CA certificate",
+			config: &mirrorConfig{URL: "https://123456789.dkr.ecr.us-east-1.amazonaws.com/myproject"},
+			want: []cabpkv1.File{
+				{
+					Path:        "/etc/containerd/certs.d/_default/hosts.toml",
+					Owner:       "",
+					Permissions: "0600",
+					Encoding:    "",
+					Append:      false,
+					Content: `[host."https://123456789.dkr.ecr.us-east-1.amazonaws.com/v2/myproject"]
+  capabilities = ["pull", "resolve"]
+  # don't rely on Containerd to add the v2/ suffix
+  # there is a bug where it is added incorrectly for mirrors with a path
+  override_path = true
 `,
 				},
 			},
@@ -51,9 +74,12 @@ func Test_generateDefaultRegistryMirrorFile(t *testing.T) {
 					Permissions: "0600",
 					Encoding:    "",
 					Append:      false,
-					Content: `[host."https://myregistry.com"]
+					Content: `[host."https://myregistry.com/v2"]
   capabilities = ["pull", "resolve"]
   ca = "/etc/certs/mirror.pem"
+  # don't rely on Containerd to add the v2/ suffix
+  # there is a bug where it is added incorrectly for mirrors with a path
+  override_path = true
 `,
 				},
 			},
diff --git a/pkg/handlers/generic/mutation/mirrors/templates/hosts.toml.gotmpl b/pkg/handlers/generic/mutation/mirrors/templates/hosts.toml.gotmpl
index 46237f6e3..41335b8dd 100644
--- a/pkg/handlers/generic/mutation/mirrors/templates/hosts.toml.gotmpl
+++ b/pkg/handlers/generic/mutation/mirrors/templates/hosts.toml.gotmpl
@@ -3,3 +3,6 @@
   {{- if .CACertPath }}
   ca = "{{ .CACertPath }}"
   {{- end }}
+  # don't rely on Containerd to add the v2/ suffix
+  # there is a bug where it is added incorrectly for mirrors with a path
+  override_path = true