diff --git a/components/common-go/experiments/flags.go b/components/common-go/experiments/flags.go
index a34b0c4bdd..4d525db4cb 100644
--- a/components/common-go/experiments/flags.go
+++ b/components/common-go/experiments/flags.go
@@ -11,6 +11,7 @@ const (
 	OIDCServiceEnabledFlag                         = "oidcServiceEnabled"
 	SupervisorPersistServerAPIChannelWhenStartFlag = "supervisor_persist_serverapi_channel_when_start"
 	SupervisorUsePublicAPIFlag                     = "supervisor_experimental_publicapi"
+	JWTSessionsEnabledFlag                         = "jwtSessionCookieEnabled"
 )
 
 func IsPersonalAccessTokensEnabled(ctx context.Context, client Client, attributes Attributes) bool {
@@ -28,3 +29,7 @@ func SupervisorPersistServerAPIChannelWhenStart(ctx context.Context, client Clie
 func SupervisorUsePublicAPI(ctx context.Context, client Client, attributes Attributes) bool {
 	return client.GetBoolValue(ctx, SupervisorUsePublicAPIFlag, false, attributes)
 }
+
+func JWTSessionsEnabled(ctx context.Context, client Client, attributes Attributes) bool {
+	return client.GetBoolValue(ctx, JWTSessionsEnabledFlag, false, attributes)
+}
diff --git a/components/public-api-server/pkg/auth/metrics.go b/components/public-api-server/pkg/auth/metrics.go
new file mode 100644
index 0000000000..38bb9f8956
--- /dev/null
+++ b/components/public-api-server/pkg/auth/metrics.go
@@ -0,0 +1,28 @@
+// Copyright (c) 2023 Gitpod GmbH. All rights reserved.
+// Licensed under the GNU Affero General Public License (AGPL).
+// See License.AGPL.txt in the project root for license information.
+
+package auth
+
+import (
+	"strconv"
+
+	"github.com/prometheus/client_golang/prometheus"
+)
+
+func reportRequestWithJWT(jwtPresent bool) {
+	requestsWithJWTSessionsTotal.WithLabelValues(strconv.FormatBool(jwtPresent)).Inc()
+}
+
+var (
+	requestsWithJWTSessionsTotal = prometheus.NewCounterVec(prometheus.CounterOpts{
+		Namespace: "gitpod",
+		Subsystem: "public_api",
+		Name:      "requests_with_jwt_sessions_total",
+		Help:      "Count of sessions with, or without JWT sessions",
+	}, []string{"with_jwt"})
+)
+
+func RegisterMetrics(registry *prometheus.Registry) {
+	registry.MustRegister(requestsWithJWTSessionsTotal)
+}
diff --git a/components/public-api-server/pkg/auth/session_jwt.go b/components/public-api-server/pkg/auth/session_jwt.go
index 5ac10e17e2..130b675e45 100644
--- a/components/public-api-server/pkg/auth/session_jwt.go
+++ b/components/public-api-server/pkg/auth/session_jwt.go
@@ -5,9 +5,14 @@
 package auth
 
 import (
+	"context"
 	"fmt"
+	"net/http"
 	"time"
 
+	"github.com/bufbuild/connect-go"
+	"github.com/gitpod-io/gitpod/common-go/experiments"
+	"github.com/gitpod-io/gitpod/common-go/log"
 	"github.com/gitpod-io/gitpod/public-api-server/pkg/jws"
 	"github.com/golang-jwt/jwt/v5"
 	"github.com/google/uuid"
@@ -41,3 +46,58 @@ func VerifySessionJWT(token string, verifier jws.Verifier, expectedIssuer string
 
 	return claims, nil
 }
+
+func NewJWTCookieInterceptor(exp experiments.Client, cookieName string, expectedIssuer string, verifier jws.Verifier) connect.UnaryInterceptorFunc {
+	interceptor := func(next connect.UnaryFunc) connect.UnaryFunc {
+
+		return connect.UnaryFunc(func(ctx context.Context, req connect.AnyRequest) (connect.AnyResponse, error) {
+			validJWT := false
+			defer func() {
+				reportRequestWithJWT(validJWT)
+			}()
+
+			if req.Spec().IsClient {
+				return next(ctx, req)
+			}
+
+			token, err := TokenFromContext(ctx)
+			if err != nil {
+				return next(ctx, req)
+			}
+
+			if !experiments.JWTSessionsEnabled(ctx, exp, experiments.Attributes{}) {
+				return next(ctx, req)
+			}
+
+			if token.Type != CookieTokenType {
+				return next(ctx, req)
+			}
+
+			jwtSessionCookie, err := cookieFromString(token.Value, cookieName)
+			if err != nil {
+				return next(ctx, req)
+			}
+
+			claims, err := VerifySessionJWT(jwtSessionCookie.Value, verifier, expectedIssuer)
+			if err != nil {
+				log.Extract(ctx).WithError(err).Warnf("Failed to verify JWT session token")
+				return next(ctx, req)
+			}
+
+			validJWT = claims != nil
+
+			return next(ctx, req)
+		})
+	}
+	return connect.UnaryInterceptorFunc(interceptor)
+}
+
+func cookieFromString(rawCookieHeader, name string) (*http.Cookie, error) {
+	// To access the cookie as an http.Cookie, we sadly have to construct a request with the appropriate header such
+	// that we can then extract the cookie.
+	header := http.Header{}
+	header.Add("Cookie", rawCookieHeader)
+	req := http.Request{Header: header}
+
+	return req.Cookie(name)
+}
diff --git a/components/public-api-server/pkg/server/server.go b/components/public-api-server/pkg/server/server.go
index 1bdca1e79f..dd6acf6070 100644
--- a/components/public-api-server/pkg/server/server.go
+++ b/components/public-api-server/pkg/server/server.go
@@ -97,7 +97,7 @@ func Start(logger *logrus.Entry, version string, cfg *config.Configuration) erro
 	if err != nil {
 		return fmt.Errorf("failed to setup JWS Keyset: %w", err)
 	}
-	_, err = jws.NewRSA256(keyset)
+	rsa256, err := jws.NewRSA256(keyset)
 	if err != nil {
 		return fmt.Errorf("failed to setup jws.RSA256: %w", err)
 	}
@@ -139,13 +139,15 @@ func Start(logger *logrus.Entry, version string, cfg *config.Configuration) erro
 	}
 
 	if registerErr := register(srv, &registerDependencies{
-		connPool:    connPool,
-		expClient:   expClient,
-		dbConn:      dbConn,
-		signer:      signer,
-		cipher:      cipherSet,
-		oidcService: oidcService,
-		idpService:  idpService,
+		connPool:        connPool,
+		expClient:       expClient,
+		dbConn:          dbConn,
+		signer:          signer,
+		cipher:          cipherSet,
+		oidcService:     oidcService,
+		idpService:      idpService,
+		authCfg:         cfg.Auth,
+		sessionVerifier: rsa256,
 	}); registerErr != nil {
 		return fmt.Errorf("failed to register services: %w", registerErr)
 	}
@@ -165,10 +167,14 @@ type registerDependencies struct {
 	cipher      db.Cipher
 	oidcService *oidc.Service
 	idpService  *identityprovider.Service
+
+	sessionVerifier jws.SignerVerifier
+	authCfg         config.AuthConfiguration
 }
 
 func register(srv *baseserver.Server, deps *registerDependencies) error {
 	proxy.RegisterMetrics(srv.MetricsRegistry())
+	auth.RegisterMetrics(srv.MetricsRegistry())
 
 	connectMetrics := NewConnectMetrics()
 	err := connectMetrics.Register(srv.MetricsRegistry())
@@ -186,6 +192,7 @@ func register(srv *baseserver.Server, deps *registerDependencies) error {
 			NewLogInterceptor(log.Log),
 			auth.NewServerInterceptor(),
 			origin.NewInterceptor(),
+			auth.NewJWTCookieInterceptor(deps.expClient, deps.authCfg.Session.Cookie.Name, deps.authCfg.Session.Issuer, deps.sessionVerifier),
 		),
 	}