diff --git a/api/api.go b/api/api.go
index 88f3bf2a..4926a324 100644
--- a/api/api.go
+++ b/api/api.go
@@ -3,9 +3,11 @@ package api
 import (
 	"context"
 	"net/http"
+	"net/url"
 	"os"
 	"os/signal"
 	"regexp"
+	"strings"
 	"syscall"
 	"time"
 
@@ -16,6 +18,7 @@ import (
 	"github.com/imdario/mergo"
 	"github.com/netlify/gotrue/conf"
 	"github.com/netlify/gotrue/mailer"
+	"github.com/netlify/gotrue/models"
 	"github.com/netlify/gotrue/storage"
 	"github.com/rs/cors"
 	"github.com/sirupsen/logrus"
@@ -219,16 +222,97 @@ func NewAPIWithVersion(ctx context.Context, globalConfig *conf.GlobalConfigurati
 		})
 	}
 
-	corsHandler := cors.New(cors.Options{
+	corsOptions := cors.Options{
 		AllowedMethods:   []string{http.MethodGet, http.MethodPost, http.MethodPut, http.MethodDelete},
 		AllowedHeaders:   []string{"Accept", "Authorization", "Content-Type", audHeaderName, useCookieHeader},
 		AllowCredentials: true,
-	})
+	}
 
-	api.handler = corsHandler.Handler(r)
+	// permissiveCors preserves the historical default: Access-Control-Allow-Origin: *.
+	// Used for instances that have not opted in to strict security.
+	permissiveCors := cors.New(corsOptions).Handler(r)
+
+	// strictCors reflects only allowlisted origins. Used per-instance when
+	// Security.Strict is set. The wrapper below stashes the resolved config on
+	// the request context so this func does not look it up again.
+	strictOptions := corsOptions
+	strictOptions.AllowOriginVaryRequestFunc = func(req *http.Request, origin string) (bool, []string) {
+		cfg := getCORSConfig(req.Context())
+		if cfg == nil {
+			return false, nil
+		}
+		return originAllowed(cfg, origin), nil
+	}
+	strictCors := cors.New(strictOptions).Handler(r)
+
+	api.handler = http.HandlerFunc(func(w http.ResponseWriter, req *http.Request) {
+		// rs/cors is a no-op when Origin is absent, so non-CORS requests can
+		// skip the per-instance resolve entirely. In multi-instance mode this
+		// is the difference between a JWS parse + DB lookup on every
+		// server-to-server request and no extra work at all.
+		if req.Header.Get("Origin") != "" {
+			if cfg := api.configForCORS(ctx, req); cfg != nil && cfg.Security.Strict {
+				strictCors.ServeHTTP(w, req.WithContext(withCORSConfig(req.Context(), cfg)))
+				return
+			}
+		}
+		permissiveCors.ServeHTTP(w, req)
+	})
 	return api
 }
 
+// configForCORS resolves the per-instance config for a CORS request. The CORS
+// wrapper runs before any per-request middleware including loadInstanceConfig,
+// so in multi-instance mode we resolve the instance config ourselves from the
+// JWS signature header.
+func (a *API) configForCORS(baseCtx context.Context, r *http.Request) *conf.Configuration {
+	if !a.config.MultiInstanceMode {
+		if cfg, ok := baseCtx.Value(configKey).(*conf.Configuration); ok {
+			return cfg
+		}
+		return nil
+	}
+	sig := r.Header.Get(jwsSignatureHeaderName)
+	if sig == "" {
+		return nil
+	}
+	claims, err := a.parseOperatorJWS(sig)
+	if err != nil || claims.InstanceID == "" {
+		return nil
+	}
+	instanceID, err := uuid.FromString(claims.InstanceID)
+	if err != nil {
+		return nil
+	}
+	instance, err := models.GetInstance(a.db, instanceID)
+	if err != nil {
+		return nil
+	}
+	cfg, err := instance.Config()
+	if err != nil {
+		return nil
+	}
+	if claims.SiteURL != "" {
+		cfg.SiteURL = claims.SiteURL
+	}
+	return cfg
+}
+
+func originAllowed(config *conf.Configuration, origin string) bool {
+	allowed := config.Security.AllowedCORSOrigins
+	if len(allowed) == 0 {
+		if su, err := url.Parse(config.SiteURL); err == nil && su.Scheme != "" && su.Host != "" {
+			allowed = []string{su.Scheme + "://" + su.Host}
+		}
+	}
+	for _, entry := range allowed {
+		if strings.EqualFold(entry, origin) {
+			return true
+		}
+	}
+	return false
+}
+
 // NewAPIFromConfigFile creates a new REST API using the provided configuration file.
 func NewAPIFromConfigFile(filename string, version string) (*API, *conf.Configuration, error) {
 	globalConfig, err := conf.LoadGlobal(filename)
diff --git a/api/api_test.go b/api/api_test.go
index c878af03..1f28da4c 100644
--- a/api/api_test.go
+++ b/api/api_test.go
@@ -2,9 +2,12 @@ package api
 
 import (
 	"context"
+	"net/http"
+	"net/http/httptest"
 	"testing"
 
 	"github.com/gofrs/uuid"
+	jwt "github.com/golang-jwt/jwt/v4"
 	"github.com/netlify/gotrue/conf"
 	"github.com/netlify/gotrue/models"
 	"github.com/netlify/gotrue/storage"
@@ -92,3 +95,156 @@ func TestEmailEnabledByDefault(t *testing.T) {
 
 	require.False(t, api.config.External.Email.Disabled)
 }
+
+// TestCORS_FlagOffPreservesWildcard guards the core safety property: when an
+// instance has not opted in, the CORS response is byte-for-byte the historical
+// default (Access-Control-Allow-Origin: *), not a reflected origin. Runs
+// without a database because preflight handling never reaches the router.
+func TestCORS_FlagOffPreservesWildcard(t *testing.T) {
+	config := &conf.Configuration{}
+	config.ApplyDefaults()
+	ctx, err := WithInstanceConfig(context.Background(), config, uuid.Nil)
+	require.NoError(t, err)
+	api := NewAPIWithVersion(ctx, &conf.GlobalConfiguration{}, nil, "test")
+
+	req := httptest.NewRequest(http.MethodOptions, "/settings", nil)
+	req.Header.Set("Origin", "https://anything.example.com")
+	req.Header.Set("Access-Control-Request-Method", "GET")
+	w := httptest.NewRecorder()
+	api.handler.ServeHTTP(w, req)
+
+	require.Equal(t, "*", w.Header().Get("Access-Control-Allow-Origin"))
+}
+
+// TestCORS_FlagOnRestrictsOrigin verifies that with Security.Strict the
+// allowlist is enforced: a non-listed origin gets no Allow-Origin header, and
+// the SiteURL origin is reflected.
+func TestCORS_FlagOnRestrictsOrigin(t *testing.T) {
+	config := &conf.Configuration{SiteURL: "https://app.example.com"}
+	config.Security.Strict = true
+	config.ApplyDefaults()
+	ctx, err := WithInstanceConfig(context.Background(), config, uuid.Nil)
+	require.NoError(t, err)
+	api := NewAPIWithVersion(ctx, &conf.GlobalConfiguration{}, nil, "test")
+
+	disallowed := httptest.NewRequest(http.MethodOptions, "/settings", nil)
+	disallowed.Header.Set("Origin", "https://evil.example.com")
+	disallowed.Header.Set("Access-Control-Request-Method", "GET")
+	wd := httptest.NewRecorder()
+	api.handler.ServeHTTP(wd, disallowed)
+	require.Empty(t, wd.Header().Get("Access-Control-Allow-Origin"))
+
+	allowed := httptest.NewRequest(http.MethodOptions, "/settings", nil)
+	allowed.Header.Set("Origin", "https://app.example.com")
+	allowed.Header.Set("Access-Control-Request-Method", "GET")
+	wa := httptest.NewRecorder()
+	api.handler.ServeHTTP(wa, allowed)
+	require.Equal(t, "https://app.example.com", wa.Header().Get("Access-Control-Allow-Origin"))
+}
+
+// TestCORS_MultiInstanceStrict exercises the multi-instance CORS path, where
+// configForCORS resolves the instance config by parsing the x-nf-sign JWS
+// header (the route middleware does not run for preflight requests). It
+// asserts the per-instance allowlist is enforced.
+func TestCORS_MultiInstanceStrict(t *testing.T) {
+	api, _, err := setupAPIForMultiinstanceTest()
+	require.NoError(t, err)
+	defer api.db.Close()
+	require.NoError(t, models.TruncateAll(api.db))
+
+	instanceID := uuid.Must(uuid.NewV4())
+	require.NoError(t, api.db.Create(&models.Instance{
+		ID:   instanceID,
+		UUID: uuid.Must(uuid.NewV4()),
+		BaseConfig: &conf.Configuration{
+			SiteURL: "https://app.example.com",
+			Security: conf.SecurityConfiguration{
+				Strict:             true,
+				AllowedCORSOrigins: []string{"https://app.example.com"},
+			},
+		},
+	}))
+
+	signature := func() string {
+		token := jwt.NewWithClaims(jwt.SigningMethodHS256, NetlifyMicroserviceClaims{
+			InstanceID: instanceID.String(),
+			SiteURL:    "https://app.example.com",
+		})
+		signed, signErr := token.SignedString([]byte(api.config.OperatorToken))
+		require.NoError(t, signErr)
+		return signed
+	}()
+
+	preflight := func(origin string) *httptest.ResponseRecorder {
+		req := httptest.NewRequest(http.MethodOptions, "/settings", nil)
+		req.Header.Set("Origin", origin)
+		req.Header.Set("Access-Control-Request-Method", "GET")
+		req.Header.Set(jwsSignatureHeaderName, signature)
+		w := httptest.NewRecorder()
+		api.handler.ServeHTTP(w, req)
+		return w
+	}
+
+	require.Equal(t, "https://app.example.com", preflight("https://app.example.com").Header().Get("Access-Control-Allow-Origin"))
+	require.Empty(t, preflight("https://evil.example.com").Header().Get("Access-Control-Allow-Origin"))
+
+	// A preflight without the signature cannot be attributed to an instance, so
+	// it falls back to the permissive (wildcard) handler.
+	noSig := httptest.NewRequest(http.MethodOptions, "/settings", nil)
+	noSig.Header.Set("Origin", "https://evil.example.com")
+	noSig.Header.Set("Access-Control-Request-Method", "GET")
+	w := httptest.NewRecorder()
+	api.handler.ServeHTTP(w, noSig)
+	require.Equal(t, "*", w.Header().Get("Access-Control-Allow-Origin"))
+}
+
+func TestOriginAllowed(t *testing.T) {
+	cases := []struct {
+		name    string
+		config  *conf.Configuration
+		origin  string
+		allowed bool
+	}{
+		{
+			name:    "matches configured allowlist",
+			config:  &conf.Configuration{Security: conf.SecurityConfiguration{AllowedCORSOrigins: []string{"https://app.example.com"}}},
+			origin:  "https://app.example.com",
+			allowed: true,
+		},
+		{
+			name:    "rejects non-listed origin",
+			config:  &conf.Configuration{Security: conf.SecurityConfiguration{AllowedCORSOrigins: []string{"https://app.example.com"}}},
+			origin:  "https://evil.com",
+			allowed: false,
+		},
+		{
+			name:    "case-insensitive match",
+			config:  &conf.Configuration{Security: conf.SecurityConfiguration{AllowedCORSOrigins: []string{"https://APP.example.com"}}},
+			origin:  "https://app.example.com",
+			allowed: true,
+		},
+		{
+			name:    "empty allowlist falls back to SiteURL origin",
+			config:  &conf.Configuration{SiteURL: "https://app.example.com/some/path"},
+			origin:  "https://app.example.com",
+			allowed: true,
+		},
+		{
+			name:    "empty allowlist rejects non-SiteURL origin",
+			config:  &conf.Configuration{SiteURL: "https://app.example.com"},
+			origin:  "https://other.example.com",
+			allowed: false,
+		},
+		{
+			name:    "empty allowlist with invalid SiteURL rejects all",
+			config:  &conf.Configuration{SiteURL: "not-a-url"},
+			origin:  "https://app.example.com",
+			allowed: false,
+		},
+	}
+	for _, tc := range cases {
+		t.Run(tc.name, func(t *testing.T) {
+			require.Equal(t, tc.allowed, originAllowed(tc.config, tc.origin))
+		})
+	}
+}
diff --git a/api/context.go b/api/context.go
index b610d309..1432cd76 100644
--- a/api/context.go
+++ b/api/context.go
@@ -29,8 +29,23 @@ const (
 	externalReferrerKey     = contextKey("external_referrer")
 	functionHooksKey        = contextKey("function_hooks")
 	adminUserKey            = contextKey("admin_user")
+	corsConfigKey           = contextKey("cors_config")
 )
 
+// withCORSConfig stashes the instance config resolved by the CORS wrapper so
+// the strict-origin check can reuse it without a second lookup.
+func withCORSConfig(ctx context.Context, config *conf.Configuration) context.Context {
+	return context.WithValue(ctx, corsConfigKey, config)
+}
+
+func getCORSConfig(ctx context.Context) *conf.Configuration {
+	obj := ctx.Value(corsConfigKey)
+	if obj == nil {
+		return nil
+	}
+	return obj.(*conf.Configuration)
+}
+
 // withToken adds the JWT token to the context.
 func withToken(ctx context.Context, token *jwt.Token) context.Context {
 	return context.WithValue(ctx, tokenKey, token)
diff --git a/api/middleware.go b/api/middleware.go
index 7573cfbd..7bb11909 100644
--- a/api/middleware.go
+++ b/api/middleware.go
@@ -100,6 +100,19 @@ func (a *API) loadJWSSignatureHeader(w http.ResponseWriter, r *http.Request) (co
 	return withSignature(ctx, signature), nil
 }
 
+// parseOperatorJWS validates the operator JWS signature and returns the claims
+// it carries. Shared by loadInstanceConfig (per-request middleware) and the
+// CORS wrapper (which runs before middleware) so signing-method and operator
+// token handling stay in one place.
+func (a *API) parseOperatorJWS(signature string) (NetlifyMicroserviceClaims, error) {
+	claims := NetlifyMicroserviceClaims{}
+	p := jwt.Parser{ValidMethods: []string{jwt.SigningMethodHS256.Name}}
+	_, err := p.ParseWithClaims(signature, &claims, func(*jwt.Token) (interface{}, error) {
+		return []byte(a.config.OperatorToken), nil
+	})
+	return claims, err
+}
+
 func (a *API) loadInstanceConfig(w http.ResponseWriter, r *http.Request) (context.Context, error) {
 	ctx := r.Context()
 
@@ -108,11 +121,7 @@ func (a *API) loadInstanceConfig(w http.ResponseWriter, r *http.Request) (contex
 		return nil, badRequestError("Operator signature missing")
 	}
 
-	claims := NetlifyMicroserviceClaims{}
-	p := jwt.Parser{ValidMethods: []string{jwt.SigningMethodHS256.Name}}
-	_, err := p.ParseWithClaims(signature, &claims, func(token *jwt.Token) (interface{}, error) {
-		return []byte(a.config.OperatorToken), nil
-	})
+	claims, err := a.parseOperatorJWS(signature)
 	if err != nil {
 		return nil, badRequestError("Operator microservice signature is invalid: %v", err)
 	}
diff --git a/conf/configuration.go b/conf/configuration.go
index 63fbdc17..ee2917c0 100644
--- a/conf/configuration.go
+++ b/conf/configuration.go
@@ -125,6 +125,10 @@ type MailerConfiguration struct {
 // follow-up changes.
 type SecurityConfiguration struct {
 	Strict bool `json:"strict"`
+
+	// AllowedCORSOrigins is the allowlist for CORS Origin when Strict.
+	// Empty list means only the SiteURL origin is accepted.
+	AllowedCORSOrigins []string `json:"allowed_cors_origins" envconfig:"ALLOWED_CORS_ORIGINS"`
 }
 
 // Configuration holds all the per-instance configuration.
diff --git a/conf/configuration_test.go b/conf/configuration_test.go
index 5e15d29e..53b96d38 100644
--- a/conf/configuration_test.go
+++ b/conf/configuration_test.go
@@ -79,6 +79,15 @@ func TestSecurityConfigurationDefaults(t *testing.T) {
 		require.NoError(t, err)
 		assert.True(t, c.Security.Strict)
 	})
+
+	t.Run("loads allowed CORS origins from env", func(t *testing.T) {
+		baseEnv()
+		os.Setenv("GOTRUE_SECURITY_STRICT", "true")
+		os.Setenv("GOTRUE_SECURITY_ALLOWED_CORS_ORIGINS", "https://app.example.com,https://preview.example.com")
+		c, err := LoadConfig("")
+		require.NoError(t, err)
+		assert.Equal(t, []string{"https://app.example.com", "https://preview.example.com"}, c.Security.AllowedCORSOrigins)
+	})
 }
 
 func TestNewInstancesSecureByDefault(t *testing.T) {