diff --git a/tests/common/auth_test.go b/tests/common/auth_test.go
index 0c34b800a3d7..e298fe0569ee 100644
--- a/tests/common/auth_test.go
+++ b/tests/common/auth_test.go
@@ -25,12 +25,16 @@ import (
 
 	clientv3 "go.etcd.io/etcd/client/v3"
 	"go.etcd.io/etcd/tests/v3/framework/config"
+	"go.etcd.io/etcd/tests/v3/framework/e2e"
 	"go.etcd.io/etcd/tests/v3/framework/testutils"
 )
 
 var tokenTTL = time.Second
+var defaultKeyPath = mustAbsPath("../fixtures/server.key.insecure")
 var defaultAuthToken = fmt.Sprintf("jwt,pub-key=%s,priv-key=%s,sign-method=RS256,ttl=%s",
-	mustAbsPath("../fixtures/server.crt"), mustAbsPath("../fixtures/server.key.insecure"), tokenTTL)
+	mustAbsPath("../fixtures/server.crt"), defaultKeyPath, tokenTTL)
+var verifyJWTOnlyAuth = fmt.Sprintf("jwt,pub-key=%s,sign-method=RS256,ttl=%s",
+	mustAbsPath("../fixtures/server.crt"), tokenTTL)
 
 const (
 	PermissionDenied      = "etcdserver: permission denied"
@@ -758,6 +762,25 @@ func TestAuthJWTExpire(t *testing.T) {
 	})
 }
 
+func TestAuthJWTOnly(t *testing.T) {
+	testRunner.BeforeTest(t)
+	ctx, cancel := context.WithTimeout(context.Background(), 30*time.Second)
+	defer cancel()
+	clus := testRunner.NewCluster(ctx, t, config.WithClusterConfig(config.ClusterConfig{ClusterSize: 1, AuthToken: verifyJWTOnlyAuth}))
+	defer clus.Close()
+	cc := testutils.MustClient(clus.Client())
+	testutils.ExecuteUntil(ctx, t, func() {
+		authRev, err := setupAuthAndGetRevision(cc, []authRole{testRole}, []authUser{rootUser, testUser})
+		require.NoErrorf(t, err, "failed to enable auth")
+
+		token, err := createSignedJWT(defaultKeyPath, testUserName, authRev)
+		require.NoErrorf(t, err, "failed to create test user JWT")
+
+		testUserAuthClient := testutils.MustClient(clus.Client(e2e.WithAuthToken(token)))
+		require.NoError(t, testUserAuthClient.Put(ctx, "foo", "bar", config.PutOptions{}))
+	})
+}
+
 // TestAuthRevisionConsistency ensures auth revision is the same after member restarts
 func TestAuthRevisionConsistency(t *testing.T) {
 	testRunner.BeforeTest(t)
diff --git a/tests/common/auth_util.go b/tests/common/auth_util.go
index 313bfb46d40e..d5da3caabfec 100644
--- a/tests/common/auth_util.go
+++ b/tests/common/auth_util.go
@@ -17,8 +17,11 @@ package common
 import (
 	"context"
 	"fmt"
+	"os"
 	"testing"
+	"time"
 
+	"github.com/golang-jwt/jwt/v4"
 	"github.com/stretchr/testify/require"
 
 	"go.etcd.io/etcd/api/v3/authpb"
@@ -93,6 +96,29 @@ func createUsers(c interfaces.Client, users []authUser) error {
 	return nil
 }
 
+func createSignedJWT(keyPath, username string, authRevision uint64) (string, error) {
+	signMethod := jwt.GetSigningMethod("RS256")
+
+	keyBytes, err := os.ReadFile(keyPath)
+	if err != nil {
+		return "", err
+	}
+
+	key, err := jwt.ParseRSAPrivateKeyFromPEM(keyBytes)
+	if err != nil {
+		return "", err
+	}
+
+	tk := jwt.NewWithClaims(signMethod,
+		jwt.MapClaims{
+			"username": username,
+			"revision": authRevision,
+			"exp":      time.Now().Add(time.Minute).Unix(),
+		})
+
+	return tk.SignedString(key)
+}
+
 func setupAuth(c interfaces.Client, roles []authRole, users []authUser) error {
 	// create roles
 	if err := createRoles(c, roles); err != nil {
@@ -107,6 +133,29 @@ func setupAuth(c interfaces.Client, roles []authRole, users []authUser) error {
 	return c.AuthEnable(context.TODO())
 }
 
+func setupAuthAndGetRevision(c interfaces.Client, roles []authRole, users []authUser) (uint64, error) {
+	// create roles
+	if err := createRoles(c, roles); err != nil {
+		return 0, err
+	}
+
+	if err := createUsers(c, users); err != nil {
+		return 0, err
+	}
+
+	// This needs to happen before enabling auth for the TestAuthJWTOnly
+	// test case because once auth is enabled we can no longer mint a valid
+	// auth token without the revision, which we won't be able to obtain
+	// without a valid auth token.
+	authrev, err := c.AuthStatus(context.TODO())
+	if err != nil {
+		return 0, err
+	}
+
+	// enable auth
+	return authrev.AuthRevision, c.AuthEnable(context.TODO())
+}
+
 func requireRolePermissionEqual(t *testing.T, expectRole authRole, actual []*authpb.Permission) {
 	require.Equal(t, 1, len(actual))
 	require.Equal(t, expectRole.permission, clientv3.PermissionType(actual[0].PermType))
diff --git a/tests/framework/e2e/etcdctl.go b/tests/framework/e2e/etcdctl.go
index 81d57c088d5c..e8d246bb3e8c 100644
--- a/tests/framework/e2e/etcdctl.go
+++ b/tests/framework/e2e/etcdctl.go
@@ -36,6 +36,7 @@ type EtcdctlV3 struct {
 	cfg        ClientConfig
 	endpoints  []string
 	authConfig clientv3.AuthConfig
+	authToken  string
 }
 
 func NewEtcdctl(cfg ClientConfig, endpoints []string, opts ...config.ClientOption) (*EtcdctlV3, error) {
@@ -73,6 +74,17 @@ func WithAuth(userName, password string) config.ClientOption {
 	}
 }
 
+func WithAuthToken(token string) config.ClientOption {
+	return func(c any) {
+		switch c := c.(type) {
+		case *EtcdctlV3:
+			c.authToken = token
+		case *clientv3.Config:
+			c.Token = token
+		}
+	}
+}
+
 func WithEndpoints(endpoints []string) config.ClientOption {
 	return func(c any) {
 		ctl := c.(*EtcdctlV3)
@@ -347,6 +359,9 @@ func (ctl *EtcdctlV3) flags() map[string]string {
 	if !ctl.authConfig.Empty() {
 		fmap["user"] = ctl.authConfig.Username + ":" + ctl.authConfig.Password
 	}
+	if ctl.authToken != "" {
+		fmap["auth-token"] = ctl.authToken
+	}
 	return fmap
 }