diff --git a/client/internal/engine.go b/client/internal/engine.go
index 1d00ed0d2..82c9d7daa 100644
--- a/client/internal/engine.go
+++ b/client/internal/engine.go
@@ -551,7 +551,7 @@ func (e *Engine) Start(netbirdConfig *mgmProto.NetbirdConfig, mgmtURL *url.URL)
 		} else {
 			log.Infof("running rosenpass in strict mode")
 		}
-		e.rpManager, err = rosenpass.NewManager(e.config.PreSharedKey, e.config.WgIfaceName, publicKey)
+		e.rpManager, err = rosenpass.NewManager(e.config.PreSharedKey, e.config.WgIfaceName, publicKey, e.config.StateDir)
 		if err != nil {
 			return fmt.Errorf("create rosenpass manager: %w", err)
 		}
diff --git a/client/internal/rosenpass/manager.go b/client/internal/rosenpass/manager.go
index 21dd751df..9d477a28b 100644
--- a/client/internal/rosenpass/manager.go
+++ b/client/internal/rosenpass/manager.go
@@ -8,6 +8,7 @@ import (
 	"log/slog"
 	"net"
 	"os"
+	"path/filepath"
 	"strconv"
 	"strings"
 	"sync"
@@ -53,9 +54,17 @@ type Manager struct {
 }
 
 // NewManager creates a new Rosenpass manager. localWgKey is the local
-// WireGuard public key, used to derive the per-peer rendezvous key.
-func NewManager(preSharedKey *wgtypes.Key, wgIfaceName string, localWgKey wgtypes.Key) (*Manager, error) {
-	public, secret, err := rp.GenerateKeyPair()
+// WireGuard public key, used to derive the per-peer rendezvous key. When stateDir
+// is non-empty the static keypair is persisted under it and reused across
+// restarts, keeping the public key (and the fingerprint peers cache) stable;
+// an empty stateDir keeps the previous behaviour of an ephemeral per-run keypair.
+func NewManager(preSharedKey *wgtypes.Key, wgIfaceName string, localWgKey wgtypes.Key, stateDir string) (*Manager, error) {
+	var keyPath string
+	if stateDir != "" {
+		keyPath = filepath.Join(stateDir, keypairFileName)
+	}
+
+	public, secret, err := loadOrGenerateKeypair(keyPath)
 	if err != nil {
 		return nil, err
 	}
diff --git a/client/internal/rosenpass/manager_test.go b/client/internal/rosenpass/manager_test.go
index 69e18ac88..8e35e7c15 100644
--- a/client/internal/rosenpass/manager_test.go
+++ b/client/internal/rosenpass/manager_test.go
@@ -255,7 +255,7 @@ func TestAddPeer_NilServer_ReturnsErrorNoCrash(t *testing.T) {
 // issue #4341 cannot occur in the window between NewManager and Run().
 func TestNewManager_PreInitializesHandler(t *testing.T) {
 	psk := wgtypes.Key{}
-	m, err := NewManager(&psk, "wt0", wgtypes.Key{0x01})
+	m, err := NewManager(&psk, "wt0", wgtypes.Key{0x01}, "")
 	require.NoError(t, err)
 	require.NotNil(t, m.rpWgHandler, "rpWgHandler must be initialized in NewManager")
 }
diff --git a/client/internal/rosenpass/persistence.go b/client/internal/rosenpass/persistence.go
new file mode 100644
index 000000000..eeb7e7f0b
--- /dev/null
+++ b/client/internal/rosenpass/persistence.go
@@ -0,0 +1,92 @@
+package rosenpass
+
+import (
+	"context"
+	"fmt"
+	"os"
+
+	rp "cunicu.li/go-rosenpass"
+	log "github.com/sirupsen/logrus"
+
+	"github.com/netbirdio/netbird/util"
+)
+
+const (
+	// keypairFileName is the file, relative to the state directory, that holds
+	// the persisted local Rosenpass static keypair.
+	keypairFileName = "rosenpass_key.json"
+
+	// rpStaticPublicKeySize is the byte length of a Rosenpass (Classic McEliece)
+	// static public key as produced by the pinned go-rosenpass version. Used as a
+	// version-compatibility guard: a persisted key of any other size is treated as
+	// stale and regenerated instead of being fed to go-rosenpass (which would fail).
+	rpStaticPublicKeySize = 524160
+
+	// keypairFormatVersion is bumped whenever the on-disk representation changes so
+	// old files are discarded and regenerated rather than misparsed.
+	keypairFormatVersion = 1
+)
+
+// persistedKeypair is the on-disk representation of the local Rosenpass static
+// keypair. Keys are stored raw (base64 via JSON) with the same restricted 0600
+// permission as the WireGuard private key and other client secrets.
+type persistedKeypair struct {
+	Version   int    `json:"version"`
+	PublicKey []byte `json:"public_key"`
+	SecretKey []byte `json:"secret_key"`
+}
+
+// loadOrGenerateKeypair returns a Rosenpass static keypair. When keyPath is set
+// and holds a valid persisted keypair it is reused, so the local public key —
+// and therefore the fingerprint advertised to remote peers over signalling —
+// stays stable across restarts. Otherwise a fresh keypair is generated and, when
+// keyPath is set, persisted for subsequent runs. A missing or corrupt file is not
+// fatal: it degrades to generating an ephemeral keypair, matching the pre-persistence
+// behaviour.
+func loadOrGenerateKeypair(keyPath string) (public []byte, secret []byte, err error) {
+	if keyPath != "" {
+		public, secret, err = loadKeypair(keyPath)
+		switch {
+		case err == nil:
+			return public, secret, nil
+		case os.IsNotExist(err):
+			// first run for this state dir; fall through to generate
+		default:
+			log.Warnf("failed to load persisted rosenpass keypair, generating a new one: %v", err)
+		}
+	}
+
+	pub, sec, err := rp.GenerateKeyPair()
+	if err != nil {
+		return nil, nil, fmt.Errorf("generate rosenpass key pair: %w", err)
+	}
+
+	if keyPath != "" {
+		if err := saveKeypair(keyPath, pub, sec); err != nil {
+			log.Warnf("failed to persist rosenpass keypair, key will be regenerated on next restart: %v", err)
+		}
+	}
+
+	return pub, sec, nil
+}
+
+func loadKeypair(keyPath string) ([]byte, []byte, error) {
+	var kp persistedKeypair
+	if _, err := util.ReadJson(keyPath, &kp); err != nil {
+		return nil, nil, err
+	}
+
+	if kp.Version != keypairFormatVersion || len(kp.PublicKey) != rpStaticPublicKeySize || len(kp.SecretKey) == 0 {
+		return nil, nil, fmt.Errorf("persisted rosenpass keypair is incompatible (version %d, public %d bytes, secret %d bytes)", kp.Version, len(kp.PublicKey), len(kp.SecretKey))
+	}
+
+	return kp.PublicKey, kp.SecretKey, nil
+}
+
+func saveKeypair(keyPath string, public, secret []byte) error {
+	return util.WriteJsonWithRestrictedPermission(context.Background(), keyPath, persistedKeypair{
+		Version:   keypairFormatVersion,
+		PublicKey: public,
+		SecretKey: secret,
+	})
+}
diff --git a/client/internal/rosenpass/persistence_test.go b/client/internal/rosenpass/persistence_test.go
new file mode 100644
index 000000000..f5c563507
--- /dev/null
+++ b/client/internal/rosenpass/persistence_test.go
@@ -0,0 +1,66 @@
+package rosenpass
+
+import (
+	"bytes"
+	"encoding/json"
+	"os"
+	"path/filepath"
+	"testing"
+
+	"github.com/stretchr/testify/require"
+)
+
+func TestLoadOrGenerateKeypair_EphemeralWhenNoPath(t *testing.T) {
+	pub, sec, err := loadOrGenerateKeypair("")
+	require.NoError(t, err)
+	require.Len(t, pub, rpStaticPublicKeySize)
+	require.NotEmpty(t, sec)
+}
+
+func TestLoadOrGenerateKeypair_PersistsAndReloads(t *testing.T) {
+	keyPath := filepath.Join(t.TempDir(), keypairFileName)
+
+	pub1, sec1, err := loadOrGenerateKeypair(keyPath)
+	require.NoError(t, err)
+
+	info, err := os.Stat(keyPath)
+	require.NoError(t, err, "keypair file must be written")
+	require.Equal(t, os.FileMode(0600), info.Mode().Perm(), "keypair file must be 0600")
+
+	pub2, sec2, err := loadOrGenerateKeypair(keyPath)
+	require.NoError(t, err)
+	require.True(t, bytes.Equal(pub1, pub2), "public key must be stable across reloads")
+	require.True(t, bytes.Equal(sec1, sec2), "secret key must be stable across reloads")
+}
+
+func TestLoadOrGenerateKeypair_RegeneratesOnCorruptFile(t *testing.T) {
+	keyPath := filepath.Join(t.TempDir(), keypairFileName)
+	require.NoError(t, os.WriteFile(keyPath, []byte("not json"), 0600))
+
+	pub, sec, err := loadOrGenerateKeypair(keyPath)
+	require.NoError(t, err)
+	require.Len(t, pub, rpStaticPublicKeySize)
+	require.NotEmpty(t, sec)
+
+	// the corrupt file must have been overwritten with a valid, reloadable keypair
+	pub2, _, err := loadOrGenerateKeypair(keyPath)
+	require.NoError(t, err)
+	require.True(t, bytes.Equal(pub, pub2))
+}
+
+func TestLoadOrGenerateKeypair_RegeneratesOnVersionMismatch(t *testing.T) {
+	keyPath := filepath.Join(t.TempDir(), keypairFileName)
+
+	pub1, _, err := loadOrGenerateKeypair(keyPath)
+	require.NoError(t, err)
+
+	// rewrite with a bumped/unknown format version -> must be discarded
+	bs, err := json.Marshal(persistedKeypair{Version: keypairFormatVersion + 1, PublicKey: pub1, SecretKey: []byte{0x01}})
+	require.NoError(t, err)
+	require.NoError(t, os.WriteFile(keyPath, bs, 0600))
+
+	pub2, sec2, err := loadOrGenerateKeypair(keyPath)
+	require.NoError(t, err)
+	require.Len(t, pub2, rpStaticPublicKeySize)
+	require.NotEmpty(t, sec2)
+}