diff --git a/internal/api/external.go b/internal/api/external.go
index f941f55e5..89f75a4fc 100644
--- a/internal/api/external.go
+++ b/internal/api/external.go
@@ -15,6 +15,7 @@ import (
 	jwt "github.com/golang-jwt/jwt/v5"
 	"github.com/sirupsen/logrus"
 	"github.com/supabase/auth/internal/api/provider"
+	"github.com/supabase/auth/internal/conf"
 	"github.com/supabase/auth/internal/models"
 	"github.com/supabase/auth/internal/observability"
 	"github.com/supabase/auth/internal/storage"
@@ -106,8 +107,7 @@ func (a *API) GetExternalProviderRedirectURL(w http.ResponseWriter, r *http.Requ
 		claims.LinkingTargetID = linkingTargetUser.ID.String()
 	}
 
-	token := jwt.NewWithClaims(jwt.SigningMethodHS256, claims)
-	tokenString, err := token.SignedString([]byte(config.JWT.Secret))
+	tokenString, err := signJwt(&config.JWT, claims)
 	if err != nil {
 		return "", internalServerError("Error creating state").WithInternalError(err)
 	}
@@ -491,9 +491,20 @@ func (a *API) loadExternalState(ctx context.Context, r *http.Request) (context.C
 	}
 	config := a.config
 	claims := ExternalProviderClaims{}
-	p := jwt.NewParser(jwt.WithValidMethods([]string{jwt.SigningMethodHS256.Name}))
+	p := jwt.NewParser(jwt.WithValidMethods(config.JWT.ValidMethods))
 	_, err := p.ParseWithClaims(state, &claims, func(token *jwt.Token) (interface{}, error) {
-		return []byte(config.JWT.Secret), nil
+		if kid, ok := token.Header["kid"]; ok {
+			if kidStr, ok := kid.(string); ok {
+				return conf.FindPublicKeyByKid(kidStr, &config.JWT)
+			}
+		}
+		if alg, ok := token.Header["alg"]; ok {
+			if alg == jwt.SigningMethodHS256.Name {
+				// preserve backward compatibility for cases where the kid is not set
+				return []byte(config.JWT.Secret), nil
+			}
+		}
+		return nil, fmt.Errorf("missing kid")
 	})
 	if err != nil {
 		return ctx, badRequestError(ErrorCodeBadOAuthState, "OAuth callback with invalid state").WithInternalError(err)
diff --git a/internal/api/jwks.go b/internal/api/jwks.go
index d03ae03fb..b8304d2dd 100644
--- a/internal/api/jwks.go
+++ b/internal/api/jwks.go
@@ -3,8 +3,10 @@ package api
 import (
 	"net/http"
 
+	jwt "github.com/golang-jwt/jwt/v5"
 	"github.com/lestrrat-go/jwx/v2/jwa"
 	jwk "github.com/lestrrat-go/jwx/v2/jwk"
+	"github.com/supabase/auth/internal/conf"
 )
 
 type JwksResponse struct {
@@ -28,3 +30,32 @@ func (a *API) Jwks(w http.ResponseWriter, r *http.Request) error {
 	w.Header().Set("Cache-Control", "public, max-age=600")
 	return sendJSON(w, http.StatusOK, resp)
 }
+
+func signJwt(config *conf.JWTConfiguration, claims jwt.Claims) (string, error) {
+	signingJwk, err := conf.GetSigningJwk(config)
+	if err != nil {
+		return "", err
+	}
+	signingMethod := conf.GetSigningAlg(signingJwk)
+	token := jwt.NewWithClaims(signingMethod, claims)
+	if token.Header == nil {
+		token.Header = make(map[string]interface{})
+	}
+
+	if _, ok := token.Header["kid"]; !ok {
+		if kid := signingJwk.KeyID(); kid != "" {
+			token.Header["kid"] = kid
+		}
+	}
+	// this serializes the aud claim to a string
+	jwt.MarshalSingleStringAsArray = false
+	signingKey, err := conf.GetSigningKey(signingJwk)
+	if err != nil {
+		return "", err
+	}
+	signed, err := token.SignedString(signingKey)
+	if err != nil {
+		return "", err
+	}
+	return signed, nil
+}
diff --git a/internal/api/token.go b/internal/api/token.go
index f9dc89829..f9a13ac00 100644
--- a/internal/api/token.go
+++ b/internal/api/token.go
@@ -349,7 +349,6 @@ func (a *API) generateAccessToken(r *http.Request, tx *storage.Connection, user
 		IsAnonymous:                   user.IsAnonymous,
 	}
 
-	var token *jwt.Token
 	var gotrueClaims jwt.Claims = claims
 	if config.Hook.CustomAccessToken.Enabled {
 		input := hooks.CustomAccessTokenInput{
@@ -367,30 +366,7 @@ func (a *API) generateAccessToken(r *http.Request, tx *storage.Connection, user
 		gotrueClaims = jwt.MapClaims(output.Claims)
 	}
 
-	signingJwk, err := conf.GetSigningJwk(&config.JWT)
-	if err != nil {
-		return "", 0, err
-	}
-
-	signingMethod := conf.GetSigningAlg(signingJwk)
-	token = jwt.NewWithClaims(signingMethod, gotrueClaims)
-	if token.Header == nil {
-		token.Header = make(map[string]interface{})
-	}
-
-	if _, ok := token.Header["kid"]; !ok {
-		if kid := signingJwk.KeyID(); kid != "" {
-			token.Header["kid"] = kid
-		}
-	}
-
-	// this serializes the aud claim to a string
-	jwt.MarshalSingleStringAsArray = false
-	signingKey, err := conf.GetSigningKey(signingJwk)
-	if err != nil {
-		return "", 0, err
-	}
-	signed, err := token.SignedString(signingKey)
+	signed, err := signJwt(&config.JWT, gotrueClaims)
 	if err != nil {
 		return "", 0, err
 	}