diff --git a/client/internal/peer/conn.go b/client/internal/peer/conn.go
index eb455431d..af6ab3f83 100644
--- a/client/internal/peer/conn.go
+++ b/client/internal/peer/conn.go
@@ -410,7 +410,7 @@ func (conn *Conn) onICEConnectionIsReady(priority conntype.ConnPriority, iceConn
 	conn.doOnConnected(iceConnInfo.RosenpassPubKey, iceConnInfo.RosenpassAddr)
 }
 
-func (conn *Conn) onICEStateDisconnected() {
+func (conn *Conn) onICEStateDisconnected(sessionChanged bool) {
 	conn.mu.Lock()
 	defer conn.mu.Unlock()
 
@@ -430,6 +430,10 @@ func (conn *Conn) onICEStateDisconnected() {
 	if conn.isReadyToUpgrade() {
 		conn.Log.Infof("ICE disconnected, set Relay to active connection")
 		conn.dumpState.SwitchToRelay()
+		if sessionChanged {
+			conn.resetEndpoint()
+		}
+
 		conn.wgProxyRelay.Work()
 
 		presharedKey := conn.presharedKey(conn.rosenpassRemoteKey)
@@ -757,6 +761,17 @@ func (conn *Conn) newProxy(remoteConn net.Conn) (wgproxy.Proxy, error) {
 	return wgProxy, nil
 }
 
+func (conn *Conn) resetEndpoint() {
+	if !isController(conn.config) {
+		return
+	}
+	conn.Log.Infof("reset wg endpoint")
+	conn.wgWatcher.Reset()
+	if err := conn.endpointUpdater.RemoveEndpointAddress(); err != nil {
+		conn.Log.Warnf("failed to remove endpoint address before update: %v", err)
+	}
+}
+
 func (conn *Conn) isReadyToUpgrade() bool {
 	return conn.wgProxyRelay != nil && conn.currentConnPriority != conntype.Relay
 }
diff --git a/client/internal/peer/endpoint.go b/client/internal/peer/endpoint.go
index 52d66159c..372f33ec6 100644
--- a/client/internal/peer/endpoint.go
+++ b/client/internal/peer/endpoint.go
@@ -66,6 +66,10 @@ func (e *EndpointUpdater) RemoveWgPeer() error {
 	return e.wgConfig.WgInterface.RemovePeer(e.wgConfig.RemoteKey)
 }
 
+func (e *EndpointUpdater) RemoveEndpointAddress() error {
+	return e.wgConfig.WgInterface.RemoveEndpointAddress(e.wgConfig.RemoteKey)
+}
+
 func (e *EndpointUpdater) waitForCloseTheDelayedUpdate() {
 	if e.cancelFunc == nil {
 		return
diff --git a/client/internal/peer/wg_watcher.go b/client/internal/peer/wg_watcher.go
index d40ec7a80..799a9375e 100644
--- a/client/internal/peer/wg_watcher.go
+++ b/client/internal/peer/wg_watcher.go
@@ -32,6 +32,8 @@ type WGWatcher struct {
 
 	enabled   bool
 	muEnabled sync.RWMutex
+
+	resetCh chan struct{}
 }
 
 func NewWGWatcher(log *log.Entry, wgIfaceStater WGInterfaceStater, peerKey string, stateDump *stateDump) *WGWatcher {
@@ -40,6 +42,7 @@ func NewWGWatcher(log *log.Entry, wgIfaceStater WGInterfaceStater, peerKey strin
 		wgIfaceStater: wgIfaceStater,
 		peerKey:       peerKey,
 		stateDump:     stateDump,
+		resetCh:       make(chan struct{}, 1),
 	}
 }
 
@@ -76,6 +79,15 @@ func (w *WGWatcher) IsEnabled() bool {
 	return w.enabled
 }
 
+// Reset signals the watcher that the WireGuard peer has been reset and a new
+// handshake is expected. This restarts the handshake timeout from scratch.
+func (w *WGWatcher) Reset() {
+	select {
+	case w.resetCh <- struct{}{}:
+	default:
+	}
+}
+
 // wgStateCheck help to check the state of the WireGuard handshake and relay connection
 func (w *WGWatcher) periodicHandshakeCheck(ctx context.Context, onDisconnectedFn func(), enabledTime time.Time, initialHandshake time.Time) {
 	w.log.Infof("WireGuard watcher started")
@@ -105,6 +117,12 @@ func (w *WGWatcher) periodicHandshakeCheck(ctx context.Context, onDisconnectedFn
 			w.stateDump.WGcheckSuccess()
 
 			w.log.Debugf("WireGuard watcher reset timer: %v", resetTime)
+		case <-w.resetCh:
+			w.log.Infof("WireGuard watcher received peer reset, restarting handshake timeout")
+			lastHandshake = time.Time{}
+			enabledTime = time.Now()
+			timer.Stop()
+			timer.Reset(wgHandshakeOvertime)
 		case <-ctx.Done():
 			w.log.Infof("WireGuard watcher stopped")
 			return
diff --git a/client/internal/peer/worker_ice.go b/client/internal/peer/worker_ice.go
index 464f57bff..edd70fb20 100644
--- a/client/internal/peer/worker_ice.go
+++ b/client/internal/peer/worker_ice.go
@@ -52,8 +52,9 @@ type WorkerICE struct {
 	// increase by one when disconnecting the agent
 	// with it the remote peer can discard the already deprecated offer/answer
 	// Without it the remote peer may recreate a workable ICE connection
-	sessionID ICESessionID
-	muxAgent  sync.Mutex
+	sessionID            ICESessionID
+	remoteSessionChanged bool
+	muxAgent             sync.Mutex
 
 	localUfrag string
 	localPwd   string
@@ -106,6 +107,7 @@ func (w *WorkerICE) OnNewOffer(remoteOfferAnswer *OfferAnswer) {
 			return
 		}
 		w.log.Debugf("agent already exists, recreate the connection")
+		w.remoteSessionChanged = true
 		w.agentDialerCancel()
 		if w.agent != nil {
 			if err := w.agent.Close(); err != nil {
@@ -306,13 +308,17 @@ func (w *WorkerICE) connect(ctx context.Context, agent *icemaker.ThreadSafeAgent
 	w.conn.onICEConnectionIsReady(selectedPriority(pair), ci)
 }
 
-func (w *WorkerICE) closeAgent(agent *icemaker.ThreadSafeAgent, cancel context.CancelFunc) {
+func (w *WorkerICE) closeAgent(agent *icemaker.ThreadSafeAgent, cancel context.CancelFunc) bool {
 	cancel()
 	if err := agent.Close(); err != nil {
 		w.log.Warnf("failed to close ICE agent: %s", err)
 	}
 
 	w.muxAgent.Lock()
+	defer w.muxAgent.Unlock()
+
+	sessionChanged := w.remoteSessionChanged
+	w.remoteSessionChanged = false
 
 	if w.agent == agent {
 		// consider to remove from here and move to the OnNewOffer
@@ -325,7 +331,7 @@ func (w *WorkerICE) closeAgent(agent *icemaker.ThreadSafeAgent, cancel context.C
 		w.agentConnecting = false
 		w.remoteSessionID = ""
 	}
-	w.muxAgent.Unlock()
+	return sessionChanged
 }
 
 func (w *WorkerICE) punchRemoteWGPort(pair *ice.CandidatePair, remoteWgPort int) {
@@ -426,11 +432,11 @@ func (w *WorkerICE) onConnectionStateChange(agent *icemaker.ThreadSafeAgent, dia
 			// ice.ConnectionStateClosed happens when we recreate the agent. For the P2P to TURN switch important to
 			// notify the conn.onICEStateDisconnected changes to update the current used priority
 
-			w.closeAgent(agent, dialerCancel)
+			sessionChanged := w.closeAgent(agent, dialerCancel)
 
 			if w.lastKnownState == ice.ConnectionStateConnected {
 				w.lastKnownState = ice.ConnectionStateDisconnected
-				w.conn.onICEStateDisconnected()
+				w.conn.onICEStateDisconnected(sessionChanged)
 			}
 		default:
 			return