diff --git a/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller.go b/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller.go
index 2223c878193b..3d4c4f30099b 100644
--- a/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller.go
+++ b/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller.go
@@ -1080,7 +1080,7 @@ func (r *HostedControlPlaneReconciler) update(ctx context.Context, hostedControl
 	}
 
 	userReleaseImageProvider := imageprovider.New(userReleaseImage)
-	releaseImageProvider := imageprovider.New(releaseImage)
+	releaseImageProvider := imageprovider.NewWithRegistryOverrides(releaseImage, r.ReleaseProvider.GetRegistryOverrides())
 
 	var errs []error
 	if err := r.reconcileCPOV2(ctx, hostedControlPlane, infraStatus, releaseImageProvider, userReleaseImageProvider); err != nil {
diff --git a/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller_test.go b/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller_test.go
index a5936e9c0454..07a2752a94a3 100644
--- a/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller_test.go
+++ b/control-plane-operator/controllers/hostedcontrolplane/hostedcontrolplane_controller_test.go
@@ -715,6 +715,8 @@ func TestEventHandling(t *testing.T) {
 	mockedProviderWithOpenshiftImageRegistryOverrides.EXPECT().
 		Lookup(gomock.Any(), gomock.Any(), gomock.Any()).
 		Return(testutils.InitReleaseImageOrDie("4.15.0"), nil).AnyTimes()
+	mockedProviderWithOpenshiftImageRegistryOverrides.EXPECT().
+		GetRegistryOverrides().Return(map[string]string{}).AnyTimes()
 	mockEC2 := awsapi.NewMockEC2API(mockCtrl)
 	mockEC2.EXPECT().DescribeVpcEndpoints(gomock.Any(), gomock.Any()).Return(&ec2.DescribeVpcEndpointsOutput{}, fmt.Errorf("not ready")).AnyTimes()
 
diff --git a/control-plane-operator/controllers/hostedcontrolplane/imageprovider/imageprovider.go b/control-plane-operator/controllers/hostedcontrolplane/imageprovider/imageprovider.go
index 9f3ee016281a..aefb8cac3dc5 100644
--- a/control-plane-operator/controllers/hostedcontrolplane/imageprovider/imageprovider.go
+++ b/control-plane-operator/controllers/hostedcontrolplane/imageprovider/imageprovider.go
@@ -1,6 +1,11 @@
 package imageprovider
 
-import "github.com/openshift/hypershift/support/releaseinfo"
+import (
+	"maps"
+
+	"github.com/openshift/hypershift/support/releaseinfo"
+	"github.com/openshift/hypershift/support/util/registryoverride"
+)
 
 //go:generate ../../../../hack/tools/bin/mockgen -source=imageprovider.go -package=imageprovider -destination=imageprovider_mock.go
 
@@ -23,11 +28,7 @@ type SimpleReleaseImageProvider struct {
 }
 
 func New(releaseImage *releaseinfo.ReleaseImage) *SimpleReleaseImageProvider {
-	return &SimpleReleaseImageProvider{
-		componentsImages: releaseImage.ComponentImages(),
-		missingImages:    make([]string, 0),
-		ReleaseImage:     releaseImage,
-	}
+	return NewWithRegistryOverrides(releaseImage, nil)
 }
 
 func NewFromImages(componentsImages map[string]string) *SimpleReleaseImageProvider {
@@ -58,3 +59,21 @@ func (p *SimpleReleaseImageProvider) ImageExist(key string) (string, bool) {
 func (p *SimpleReleaseImageProvider) ComponentImages() map[string]string {
 	return p.componentsImages
 }
+
+// NewWithRegistryOverrides creates a SimpleReleaseImageProvider that applies
+// registry overrides to all component images. This ensures init containers
+// and other sub-resources created by CPO use the overridden image references.
+//
+// The returned provider owns a private copy of releaseImage.ComponentImages()
+// so callers can safely mutate it.
+func NewWithRegistryOverrides(releaseImage *releaseinfo.ReleaseImage, registryOverrides map[string]string) *SimpleReleaseImageProvider {
+	images := maps.Clone(releaseImage.ComponentImages())
+	for key, image := range images {
+		images[key] = registryoverride.Replace(image, registryOverrides)
+	}
+	return &SimpleReleaseImageProvider{
+		componentsImages: images,
+		missingImages:    make([]string, 0),
+		ReleaseImage:     releaseImage,
+	}
+}
diff --git a/support/releaseinfo/registry_mirror_provider.go b/support/releaseinfo/registry_mirror_provider.go
index e1b8803ae9fb..61efd1f2f081 100644
--- a/support/releaseinfo/registry_mirror_provider.go
+++ b/support/releaseinfo/registry_mirror_provider.go
@@ -2,8 +2,9 @@ package releaseinfo
 
 import (
 	"context"
-	"strings"
 	"sync"
+
+	"github.com/openshift/hypershift/support/util/registryoverride"
 )
 
 var _ ProviderWithRegistryOverrides = (*RegistryMirrorProviderDecorator)(nil)
@@ -34,9 +35,7 @@ func (p *RegistryMirrorProviderDecorator) Lookup(ctx context.Context, image stri
 
 	imageStream := releaseImage.ImageStream.DeepCopy() // deepCopy so the cache is not overridden.
 	for i := range imageStream.Spec.Tags {
-		for registrySource, registryDest := range p.RegistryOverrides {
-			imageStream.Spec.Tags[i].From.Name = strings.Replace(imageStream.Spec.Tags[i].From.Name, registrySource, registryDest, 1)
-		}
+		imageStream.Spec.Tags[i].From.Name = registryoverride.Replace(imageStream.Spec.Tags[i].From.Name, p.RegistryOverrides)
 	}
 
 	return &ReleaseImage{
diff --git a/support/util/registryoverride/registryoverride.go b/support/util/registryoverride/registryoverride.go
new file mode 100644
index 000000000000..e7eff74bad49
--- /dev/null
+++ b/support/util/registryoverride/registryoverride.go
@@ -0,0 +1,68 @@
+// Package registryoverride applies registry-prefix overrides to image
+// references with strict, deterministic matching semantics. It is intentionally
+// a leaf package with no project-internal imports so it can be used both from
+// support/releaseinfo and from sub-packages that depend on it.
+package registryoverride
+
+import "strings"
+
+// Replace remaps an image reference using a set of registry-prefix overrides.
+// The overrides map keys are source registry prefixes and values are
+// replacement prefixes.
+//
+// Matching is strict: an override applies only when the image reference is
+// exactly equal to the source key or starts with the source key followed by a
+// valid image-reference separator ("/" for path components, "@" for digests,
+// or ":" for tags). This prevents accidental substring matches (e.g. an
+// override for "quay.io" must not match "quay.io.example.com/foo") while
+// correctly handling repository-level overrides against digest references
+// (e.g. "quay.io/org/repo" must match "quay.io/org/repo@sha256:abc").
+//
+// When several override keys match the same image, the longest key wins. This
+// makes the result deterministic regardless of map iteration order and lets
+// callers express both broad ("quay.io") and narrow
+// ("quay.io/openshift-release-dev") overrides simultaneously.
+//
+// If no override matches, image is returned unchanged.
+func Replace(image string, overrides map[string]string) string {
+	if image == "" || len(overrides) == 0 {
+		return image
+	}
+
+	var bestSource, bestTarget string
+	for source, target := range overrides {
+		if source == "" {
+			continue
+		}
+		if !matchesPrefix(image, source) {
+			continue
+		}
+		if len(source) > len(bestSource) {
+			bestSource, bestTarget = source, target
+		}
+	}
+	if bestSource == "" {
+		return image
+	}
+	return bestTarget + image[len(bestSource):]
+}
+
+// matchesPrefix reports whether image is exactly source, or source is a prefix
+// of image followed by a valid separator. Valid separators are "/" (path) and
+// "@" (digest), always. ":" is accepted only when source contains a "/" (i.e.
+// includes a path component), where it denotes a tag boundary. Without a "/"
+// the source is a bare hostname and ":" would be a port separator, which must
+// not match (e.g. override "quay.io" must not match "quay.io:5000/foo").
+func matchesPrefix(image, source string) bool {
+	if image == source {
+		return true
+	}
+	if !strings.HasPrefix(image, source) {
+		return false
+	}
+	sep := image[len(source)]
+	if sep == '/' || sep == '@' {
+		return true
+	}
+	return sep == ':' && strings.ContainsRune(source, '/')
+}
diff --git a/support/util/registryoverride/registryoverride_test.go b/support/util/registryoverride/registryoverride_test.go
new file mode 100644
index 000000000000..1212c8ae9b74
--- /dev/null
+++ b/support/util/registryoverride/registryoverride_test.go
@@ -0,0 +1,170 @@
+package registryoverride
+
+import (
+	"reflect"
+	"testing"
+)
+
+func TestReplace(t *testing.T) {
+	t.Parallel()
+
+	cases := []struct {
+		name      string
+		image     string
+		overrides map[string]string
+		want      string
+	}{
+		{
+			name:      "nil overrides returns input unchanged",
+			image:     "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+			overrides: nil,
+			want:      "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+		},
+		{
+			name:      "empty overrides returns input unchanged",
+			image:     "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+			overrides: map[string]string{},
+			want:      "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+		},
+		{
+			name:      "no matching override returns input unchanged",
+			image:     "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+			overrides: map[string]string{"registry.redhat.io": "mirror.example.com"},
+			want:      "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+		},
+		{
+			name:      "exact-match key replaces image",
+			image:     "quay.io",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "mirror.example.com",
+		},
+		{
+			name:      "slash-boundary prefix match preserves path and digest",
+			image:     "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "mirror.example.com/openshift-release-dev/ocp-release@sha256:abc",
+		},
+		{
+			name:      "subdomain does not match (no false positive)",
+			image:     "quay.io.example.com/foo/bar:latest",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "quay.io.example.com/foo/bar:latest",
+		},
+		{
+			name:      "trailing path component does not match (no false positive)",
+			image:     "quay.io-evil/foo:latest",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "quay.io-evil/foo:latest",
+		},
+		{
+			name:  "longest matching prefix wins",
+			image: "quay.io/openshift-release-dev/ocp-release@sha256:abc",
+			overrides: map[string]string{
+				"quay.io":                       "broad.example.com",
+				"quay.io/openshift-release-dev": "narrow.example.com/mirror",
+			},
+			want: "narrow.example.com/mirror/ocp-release@sha256:abc",
+		},
+		{
+			name:  "shorter prefix used when longer prefix does not match",
+			image: "quay.io/some-other-org/image:tag",
+			overrides: map[string]string{
+				"quay.io":                       "broad.example.com",
+				"quay.io/openshift-release-dev": "narrow.example.com/mirror",
+			},
+			want: "broad.example.com/some-other-org/image:tag",
+		},
+		{
+			name:  "empty source key is skipped",
+			image: "quay.io/foo/bar:latest",
+			overrides: map[string]string{
+				"":        "should-never-be-used",
+				"quay.io": "mirror.example.com",
+			},
+			want: "mirror.example.com/foo/bar:latest",
+		},
+		{
+			name:      "tag is preserved",
+			image:     "quay.io/foo/bar:v1.2.3",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "mirror.example.com/foo/bar:v1.2.3",
+		},
+		{
+			name:      "When source matches full repository with digest separator it should replace prefix",
+			image:     "quay.io/openshift-release-dev/ocp-v4.0-art-dev@sha256:abc123",
+			overrides: map[string]string{"quay.io/openshift-release-dev/ocp-v4.0-art-dev": "mirror.example.com/art-dev"},
+			want:      "mirror.example.com/art-dev@sha256:abc123",
+		},
+		{
+			name:      "When source matches full repository with tag separator it should replace prefix",
+			image:     "quay.io/openshift-release-dev/ocp-v4.0-art-dev:latest",
+			overrides: map[string]string{"quay.io/openshift-release-dev/ocp-v4.0-art-dev": "mirror.example.com/art-dev"},
+			want:      "mirror.example.com/art-dev:latest",
+		},
+		{
+			name:  "When multiple overrides match with digest it should pick longest prefix",
+			image: "quay.io/openshift-release-dev/ocp-v4.0-art-dev@sha256:abc123",
+			overrides: map[string]string{
+				"quay.io": "broad.example.com",
+				"quay.io/openshift-release-dev/ocp-v4.0-art-dev": "narrow.example.com/art-dev",
+			},
+			want: "narrow.example.com/art-dev@sha256:abc123",
+		},
+		{
+			name:      "When source has trailing dash it should not match similar prefix (no false positive)",
+			image:     "quay.io/openshift-release-dev/ocp-v4.0-art-dev-extra@sha256:abc",
+			overrides: map[string]string{"quay.io/openshift-release-dev/ocp-v4.0-art-dev": "mirror/art-dev"},
+			want:      "quay.io/openshift-release-dev/ocp-v4.0-art-dev-extra@sha256:abc",
+		},
+		{
+			name:      "When host-only source matches host:port image it should not match (port is not a tag)",
+			image:     "quay.io:5000/org/repo@sha256:abc",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "quay.io:5000/org/repo@sha256:abc",
+		},
+		{
+			name:      "When host:port source matches host:port image it should match via slash",
+			image:     "myregistry:5000/org/repo@sha256:abc",
+			overrides: map[string]string{"myregistry:5000": "mirror.example.com"},
+			want:      "mirror.example.com/org/repo@sha256:abc",
+		},
+		{
+			name:      "empty image returns empty",
+			image:     "",
+			overrides: map[string]string{"quay.io": "mirror.example.com"},
+			want:      "",
+		},
+	}
+
+	for _, tc := range cases {
+		t.Run(tc.name, func(t *testing.T) {
+			t.Parallel()
+			got := Replace(tc.image, tc.overrides)
+			if got != tc.want {
+				t.Errorf("Replace(%q, %v) = %q, want %q", tc.image, tc.overrides, got, tc.want)
+			}
+		})
+	}
+}
+
+func TestReplace_DoesNotMutateOverrides(t *testing.T) {
+	t.Parallel()
+
+	overrides := map[string]string{
+		"quay.io":                       "broad.example.com",
+		"quay.io/openshift-release-dev": "narrow.example.com/mirror",
+		"registry.redhat.io":            "rh.mirror.example.com",
+	}
+	snapshot := make(map[string]string, len(overrides))
+	for k, v := range overrides {
+		snapshot[k] = v
+	}
+
+	_ = Replace("quay.io/openshift-release-dev/ocp-release@sha256:abc", overrides)
+	_ = Replace("registry.redhat.io/some/image:latest", overrides)
+	_ = Replace("does.not.match/anything:tag", overrides)
+
+	if !reflect.DeepEqual(overrides, snapshot) {
+		t.Errorf("overrides map was mutated by Replace; got %v, want %v", overrides, snapshot)
+	}
+}