diff --git a/api/types/role.go b/api/types/role.go
index 98263f1973d4f..fd29e06fca395 100644
--- a/api/types/role.go
+++ b/api/types/role.go
@@ -1836,9 +1836,10 @@ func setDefaultKubernetesVerbs(spec *RoleSpecV6) {
 // - Namespace is not empty
 func validateKubeResources(roleVersion string, kubeResources []KubernetesResource) error {
 	for _, kubeResource := range kubeResources {
-		if !slices.Contains(KubernetesResourcesKinds, kubeResource.Kind) && kubeResource.Kind != Wildcard {
-			return trace.BadParameter("KubernetesResource kind %q is invalid or unsupported; Supported: %v", kubeResource.Kind, append([]string{Wildcard}, KubernetesResourcesKinds...))
-		}
+		// TODO(creack): Move the validation to the server side so we can lookup the list of valid CRDs.
+		// if !slices.Contains(KubernetesResourcesKinds, kubeResource.Kind) && kubeResource.Kind != Wildcard {
+		// 	return trace.BadParameter("KubernetesResource kind %q is invalid or unsupported; Supported: %v", kubeResource.Kind, append([]string{Wildcard}, KubernetesResourcesKinds...))
+		// }
 
 		for _, verb := range kubeResource.Verbs {
 			if !slices.Contains(KubernetesVerbs, verb) && verb != Wildcard && !strings.Contains(verb, "{{") {
diff --git a/lib/kube/proxy/forwarder.go b/lib/kube/proxy/forwarder.go
index b3df6d6c0b153..f2303ec1e6162 100644
--- a/lib/kube/proxy/forwarder.go
+++ b/lib/kube/proxy/forwarder.go
@@ -30,6 +30,7 @@ import (
 	"net"
 	"net/http"
 	"net/url"
+	"path"
 	"slices"
 	"strconv"
 	"strings"
@@ -801,6 +802,9 @@ func (f *Forwarder) setupContext(
 			return nil, trace.Wrap(err)
 		}
 	}
+	if kubeResource != nil && kubeResource.Kind == "CustomResource" {
+		kubeResource.Kind = path.Join(apiResource.apiGroup, apiResource.apiGroupVersion, apiResource.resourceKind)
+	}
 
 	netConfig, err := f.cfg.CachingAuthClient.GetClusterNetworkingConfig(f.ctx)
 	if err != nil {
diff --git a/lib/kube/proxy/resource_list.go b/lib/kube/proxy/resource_list.go
index d0401a600fe5d..63bfd2f4eb57d 100644
--- a/lib/kube/proxy/resource_list.go
+++ b/lib/kube/proxy/resource_list.go
@@ -22,6 +22,7 @@ import (
 	"bytes"
 	"io"
 	"net/http"
+	"path"
 	"strings"
 	"sync"
 	"time"
@@ -59,6 +60,9 @@ func (f *Forwarder) listResources(sess *clusterSession, w http.ResponseWriter, r
 	if isLocalKubeCluster {
 		resourceKind, supportsType = sess.rbacSupportedResources.getTeleportResourceKindFromAPIResource(sess.apiResource)
 	}
+	if resourceKind == "CustomResource" {
+		resourceKind = path.Join(sess.apiResource.apiGroup, sess.apiResource.apiGroupVersion, sess.apiResource.resourceKind)
+	}
 
 	// status holds the returned response code.
 	var status int
@@ -119,6 +123,9 @@ func (f *Forwarder) listResourcesList(req *http.Request, w http.ResponseWriter,
 	if !ok {
 		return http.StatusBadRequest, trace.BadParameter("unknown resource kind %q", sess.apiResource.resourceKind)
 	}
+	if resourceKind == "CustomResource" {
+		resourceKind = path.Join(sess.apiResource.apiGroup, sess.apiResource.apiGroupVersion, sess.apiResource.resourceKind)
+	}
 	verb := sess.requestVerb
 	// filterBuffer filters the response to exclude resources the user doesn't have access to.
 	// The filtered payload will be written into memBuffer again.