diff --git a/tests/common/auth_test.go b/tests/common/auth_test.go
index 0c34b800a..7f120bfad 100644
--- a/tests/common/auth_test.go
+++ b/tests/common/auth_test.go
@@ -29,8 +29,11 @@ import (
 )
 
 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 +761,25 @@ 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, "RS256", testUserName, authRev)
+		require.NoErrorf(t, err, "failed to create test user JWT")
+
+		testUserAuthClient := testutils.MustClient(clus.Client(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 313bfb46d..a4013822c 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, alg, username string, authRevision uint64) (string, error) {
+	signMethod := jwt.GetSigningMethod(alg)
+
+	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/common/e2e_test.go b/tests/common/e2e_test.go
index 11c4f94a3..e9e2f1921 100644
--- a/tests/common/e2e_test.go
+++ b/tests/common/e2e_test.go
@@ -78,6 +78,10 @@ func WithAuth(userName, password string) config.ClientOption {
 	return e2e.WithAuth(userName, password)
 }
 
+func WithAuthToken(token string) config.ClientOption {
+	return e2e.WithAuthToken(token)
+}
+
 func WithEndpoints(endpoints []string) config.ClientOption {
 	return e2e.WithEndpoints(endpoints)
 }
diff --git a/tests/common/integration_test.go b/tests/common/integration_test.go
index c4cabeeb1..f41055c44 100644
--- a/tests/common/integration_test.go
+++ b/tests/common/integration_test.go
@@ -56,6 +56,10 @@ func WithAuth(userName, password string) config.ClientOption {
 	return integration.WithAuth(userName, password)
 }
 
+func WithAuthToken(token string) config.ClientOption {
+	return integration.WithAuthToken(token)
+}
+
 func WithEndpoints(endpoints []string) config.ClientOption {
 	return integration.WithEndpoints(endpoints)
 }
diff --git a/tests/common/unit_test.go b/tests/common/unit_test.go
index 4b172e7a3..48e3a51cd 100644
--- a/tests/common/unit_test.go
+++ b/tests/common/unit_test.go
@@ -37,6 +37,10 @@ func WithAuth(userName, password string) config.ClientOption {
 	return func(any) {}
 }
 
+func WithAuthToken(token string) config.ClientOption {
+	return func(any) {}
+}
+
 func WithEndpoints(endpoints []string) config.ClientOption {
 	return func(any) {}
 }
diff --git a/tests/framework/e2e/etcdctl.go b/tests/framework/e2e/etcdctl.go
index 81d57c088..e9266cfb2 100644
--- a/tests/framework/e2e/etcdctl.go
+++ b/tests/framework/e2e/etcdctl.go
@@ -55,6 +55,7 @@ func NewEtcdctl(cfg ClientConfig, endpoints []string, opts ...config.ClientOptio
 			DialOptions: []grpc.DialOption{grpc.WithBlock()},
 			Username:    ctl.authConfig.Username,
 			Password:    ctl.authConfig.Password,
+			Token:       ctl.authConfig.Token,
 		})
 		if err != nil {
 			return nil, err
@@ -73,6 +74,13 @@ func WithAuth(userName, password string) config.ClientOption {
 	}
 }
 
+func WithAuthToken(token string) config.ClientOption {
+	return func(c any) {
+		ctl := c.(*EtcdctlV3)
+		ctl.authConfig.Token = token
+	}
+}
+
 func WithEndpoints(endpoints []string) config.ClientOption {
 	return func(c any) {
 		ctl := c.(*EtcdctlV3)
@@ -344,7 +352,9 @@ func (ctl *EtcdctlV3) flags() map[string]string {
 		}
 	}
 	fmap["endpoints"] = strings.Join(ctl.endpoints, ",")
-	if !ctl.authConfig.Empty() {
+	if ctl.authConfig.Token != "" {
+		fmap["auth-jwt-token"] = ctl.authConfig.Token
+	} else if !ctl.authConfig.Empty() {
 		fmap["user"] = ctl.authConfig.Username + ":" + ctl.authConfig.Password
 	}
 	return fmap
diff --git a/tests/framework/integration/cluster.go b/tests/framework/integration/cluster.go
index 95b5c88d9..a164fcc72 100644
--- a/tests/framework/integration/cluster.go
+++ b/tests/framework/integration/cluster.go
@@ -1478,6 +1478,13 @@ func WithAuth(userName, password string) framecfg.ClientOption {
 	}
 }
 
+func WithAuthToken(token string) framecfg.ClientOption {
+	return func(c any) {
+		cfg := c.(*clientv3.Config)
+		cfg.Token = token
+	}
+}
+
 func WithEndpoints(endpoints []string) framecfg.ClientOption {
 	return func(c any) {
 		cfg := c.(*clientv3.Config)
diff --git a/tests/go.mod b/tests/go.mod
index 57e6b857e..2ca1ad816 100644
--- a/tests/go.mod
+++ b/tests/go.mod
@@ -18,6 +18,7 @@ replace (
 require (
 	github.com/anishathalye/porcupine v0.1.4
 	github.com/coreos/go-semver v0.3.1
+	github.com/golang-jwt/jwt/v4 v4.5.0
 	github.com/golang/protobuf v1.5.4
 	github.com/google/go-cmp v0.6.0
 	github.com/grpc-ecosystem/go-grpc-middleware v1.3.0
@@ -65,7 +66,6 @@ require (
 	github.com/go-logr/logr v1.4.2 // indirect
 	github.com/go-logr/stdr v1.2.2 // indirect
 	github.com/gogo/protobuf v1.3.2 // indirect
-	github.com/golang-jwt/jwt/v4 v4.5.0 // indirect
 	github.com/golang/groupcache v0.0.0-20210331224755-41bb18bfe9da // indirect
 	github.com/google/btree v1.1.2 // indirect
 	github.com/google/uuid v1.6.0 // indirect