diff --git a/cmd/kube-apiserver/app/options/validation.go b/cmd/kube-apiserver/app/options/validation.go
index 38250a7a819..d96a6a41b17 100644
--- a/cmd/kube-apiserver/app/options/validation.go
+++ b/cmd/kube-apiserver/app/options/validation.go
@@ -124,10 +124,11 @@ func validateTokenRequest(options *ServerRunOptions) []error {
 
 func validateAPIPriorityAndFairness(options *ServerRunOptions) []error {
 	if utilfeature.DefaultFeatureGate.Enabled(genericfeatures.APIPriorityAndFairness) && options.GenericServerRunOptions.EnablePriorityAndFairness {
-		// If none of the following runtime config options are specified, APF is
-		// assumed to be turned on.
+		// If none of the following runtime config options are specified,
+		// APF is assumed to be turned on. The internal APF controller uses
+		// v1beta3 so it should be enabled.
 		enabledAPIString := options.APIEnablement.RuntimeConfig.String()
-		testConfigs := []string{"flowcontrol.apiserver.k8s.io/v1beta2", "flowcontrol.apiserver.k8s.io/v1beta1", "api/beta", "api/all"} // in the order of precedence
+		testConfigs := []string{"flowcontrol.apiserver.k8s.io/v1beta3", "api/beta", "api/all"} // in the order of precedence
 		for _, testConfig := range testConfigs {
 			if strings.Contains(enabledAPIString, fmt.Sprintf("%s=false", testConfig)) {
 				return []error{fmt.Errorf("--runtime-config=%s=false conflicts with --enable-priority-and-fairness=true and --feature-gates=APIPriorityAndFairness=true", testConfig)}
diff --git a/cmd/kube-apiserver/app/options/validation_test.go b/cmd/kube-apiserver/app/options/validation_test.go
index 1a997a43317..e77517e372a 100644
--- a/cmd/kube-apiserver/app/options/validation_test.go
+++ b/cmd/kube-apiserver/app/options/validation_test.go
@@ -18,9 +18,11 @@ package options
 
 import (
 	"net"
+	"strings"
 	"testing"
 
 	utilnet "k8s.io/apimachinery/pkg/util/net"
+	genericoptions "k8s.io/apiserver/pkg/server/options"
 	netutils "k8s.io/utils/net"
 )
 
@@ -250,3 +252,52 @@ func TestValidateMaxCIDRRange(t *testing.T) {
 		})
 	}
 }
+
+func TestValidateAPIPriorityAndFairness(t *testing.T) {
+	const conflict = "conflicts with --enable-priority-and-fairness=true and --feature-gates=APIPriorityAndFairness=true"
+	tests := []struct {
+		runtimeConfig    string
+		errShouldContain string
+	}{
+		{
+			runtimeConfig:    "api/all=false",
+			errShouldContain: conflict,
+		},
+		{
+			runtimeConfig:    "api/beta=false",
+			errShouldContain: conflict,
+		},
+		{
+			runtimeConfig:    "flowcontrol.apiserver.k8s.io/v1beta1=false",
+			errShouldContain: "",
+		},
+		{
+			runtimeConfig:    "flowcontrol.apiserver.k8s.io/v1beta2=false",
+			errShouldContain: "",
+		},
+		{
+			runtimeConfig:    "flowcontrol.apiserver.k8s.io/v1beta3=false",
+			errShouldContain: conflict,
+		},
+	}
+
+	for _, test := range tests {
+		t.Run(test.runtimeConfig, func(t *testing.T) {
+			options := &ServerRunOptions{
+				GenericServerRunOptions: &genericoptions.ServerRunOptions{
+					EnablePriorityAndFairness: true,
+				},
+				APIEnablement: genericoptions.NewAPIEnablementOptions(),
+			}
+			options.APIEnablement.RuntimeConfig.Set(test.runtimeConfig)
+
+			var errMessageGot string
+			if errs := validateAPIPriorityAndFairness(options); len(errs) > 0 {
+				errMessageGot = errs[0].Error()
+			}
+			if !strings.Contains(errMessageGot, test.errShouldContain) {
+				t.Errorf("Expected error message to contain: %q, but got: %q", test.errShouldContain, errMessageGot)
+			}
+		})
+	}
+}