diff --git a/internal/start/start.go b/internal/start/start.go
index bcc2cde48..1184b6590 100644
--- a/internal/start/start.go
+++ b/internal/start/start.go
@@ -4,6 +4,7 @@ import (
 	"bytes"
 	"context"
 	_ "embed"
+	"encoding/json"
 	"fmt"
 	"io"
 	"net"
@@ -621,8 +622,8 @@ EOF
 			fmt.Sprintf("GOTRUE_RATE_LIMIT_WEB3=%v", utils.Config.Auth.RateLimit.Web3),
 		}
 
-		// Since signing key is validated by ResolveJWKS, simply read the key file.
-		if keys, err := afero.ReadFile(fsys, utils.Config.Auth.SigningKeysPath); err == nil && len(keys) > 0 {
+		// Serialise default or custom signing keys
+		if keys, err := json.Marshal(utils.Config.Auth.SigningKeys); err == nil {
 			env = append(env, "GOTRUE_JWT_KEYS="+string(keys))
 			// TODO: deprecate HS256 when it's no longer supported
 			env = append(env, "GOTRUE_JWT_VALID_METHODS=HS256,RS256,ES256")
diff --git a/pkg/config/apikeys.go b/pkg/config/apikeys.go
index 12ecb2076..a5f6ee1de 100644
--- a/pkg/config/apikeys.go
+++ b/pkg/config/apikeys.go
@@ -4,6 +4,7 @@ import (
 	"crypto"
 	"crypto/ecdsa"
 	"crypto/elliptic"
+	"crypto/rand"
 	"crypto/rsa"
 	"encoding/base64"
 	"math/big"
@@ -11,6 +12,8 @@ import (
 
 	"github.com/go-errors/errors"
 	"github.com/golang-jwt/jwt/v5"
+	"github.com/google/uuid"
+	"github.com/supabase/cli/pkg/cast"
 )
 
 const (
@@ -46,6 +49,25 @@ func (a *auth) generateAPIKeys() error {
 	} else if len(a.JwtSecret.Value) < 16 {
 		return errors.Errorf("Invalid config for auth.jwt_secret. Must be at least 16 characters")
 	}
+	// Generate default signing key (P-256 curve for ES256)
+	if len(a.SigningKeysPath) == 0 {
+		privateKey, err := ecdsa.GenerateKey(elliptic.P256(), rand.Reader)
+		if err != nil {
+			return errors.Errorf("failed to generate ECDSA key: %w", err)
+		}
+		a.SigningKeys = append(a.SigningKeys, JWK{
+			KeyType:         "EC",
+			KeyID:           uuid.New().String(),
+			Use:             "sig",
+			KeyOps:          []string{"sign", "verify"},
+			Algorithm:       "ES256",
+			Extractable:     cast.Ptr(true),
+			Curve:           "P-256",
+			X:               base64.RawURLEncoding.EncodeToString(privateKey.PublicKey.X.Bytes()),
+			Y:               base64.RawURLEncoding.EncodeToString(privateKey.PublicKey.Y.Bytes()),
+			PrivateExponent: base64.RawURLEncoding.EncodeToString(privateKey.D.Bytes()),
+		})
+	}
 	// Generate anon key if not provided
 	if len(a.AnonKey.Value) == 0 {
 		signed, err := a.generateJWT("anon")
diff --git a/pkg/config/config.go b/pkg/config/config.go
index 6e9ef96bb..3c88e0340 100644
--- a/pkg/config/config.go
+++ b/pkg/config/config.go
@@ -1538,7 +1538,7 @@ func (a *auth) ResolveJWKS(ctx context.Context) (string, error) {
 		jwks.Keys = append(jwks.Keys, json.RawMessage(publicKeyEncoded))
 	}
 	// Fallback to JWT_SECRET for backward compatibility
-	if len(a.SigningKeys) == 0 {
+	if len(a.SigningKeysPath) == 0 {
 		jwtSecret := secretJWK{
 			KeyType:      "oct",
 			KeyBase64URL: base64.RawURLEncoding.EncodeToString([]byte(a.JwtSecret.Value)),