diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 6ffc59891..b071120ce 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -215,7 +215,7 @@ func NewLocalBackend(logf logger.Logf, logid string, store ipn.StateStore, diale
 	wiredPeerAPIPort := false
 	if ig, ok := e.(wgengine.InternalsGetter); ok {
 		if tunWrap, _, ok := ig.GetInternals(); ok {
-			tunWrap.PeerAPIPort = b.getPeerAPIPortForTSMPPing
+			tunWrap.PeerAPIPort = b.GetPeerAPIPort
 			wiredPeerAPIPort = true
 		}
 	}
@@ -1788,7 +1788,9 @@ func (b *LocalBackend) setPrefsLockedOnEntry(caller string, newp *ipn.Prefs) {
 	b.send(ipn.Notify{Prefs: newp})
 }
 
-func (b *LocalBackend) getPeerAPIPortForTSMPPing(ip netaddr.IP) (port uint16, ok bool) {
+// GetPeerAPIPort returns the port number for the peerapi server
+// running on the provided IP.
+func (b *LocalBackend) GetPeerAPIPort(ip netaddr.IP) (port uint16, ok bool) {
 	b.mu.Lock()
 	defer b.mu.Unlock()
 	for _, pln := range b.peerAPIListeners {
@@ -1799,6 +1801,27 @@ func (b *LocalBackend) getPeerAPIPortForTSMPPing(ip netaddr.IP) (port uint16, ok
 	return 0, false
 }
 
+// ServePeerAPIConnection serves an already-accepted connection c.
+//
+// The remote parameter is the remote address.
+// The local paramater is the local address (either a Tailscale IPv4
+// or IPv6 IP and the peerapi port for that address).
+//
+// The connection will be closed by ServePeerAPIConnection.
+func (b *LocalBackend) ServePeerAPIConnection(remote, local netaddr.IPPort, c net.Conn) {
+	b.mu.Lock()
+	defer b.mu.Unlock()
+	for _, pln := range b.peerAPIListeners {
+		if pln.ip == local.IP() {
+			go pln.ServeConn(remote, c)
+			return
+		}
+	}
+	b.logf("[unexpected] no peerAPI listener found for %v", local)
+	c.Close()
+	return
+}
+
 func (b *LocalBackend) peerAPIServicesLocked() (ret []tailcfg.Service) {
 	for _, pln := range b.peerAPIListeners {
 		proto := tailcfg.PeerAPI4
diff --git a/ipn/ipnlocal/peerapi.go b/ipn/ipnlocal/peerapi.go
index 19aeb2240..8c2fe946b 100644
--- a/ipn/ipnlocal/peerapi.go
+++ b/ipn/ipnlocal/peerapi.go
@@ -481,29 +481,34 @@ func (pln *peerAPIListener) serve() {
 			c.Close()
 			continue
 		}
-		peerNode, peerUser, ok := pln.lb.WhoIs(ipp)
-		if !ok {
-			logf("peerapi: unknown peer %v", ipp)
-			c.Close()
-			continue
-		}
-		h := &peerAPIHandler{
-			ps:         pln.ps,
-			isSelf:     pln.ps.selfNode.User == peerNode.User,
-			remoteAddr: ipp,
-			peerNode:   peerNode,
-			peerUser:   peerUser,
-		}
-		httpServer := &http.Server{
-			Handler: h,
-		}
-		if addH2C != nil {
-			addH2C(httpServer)
-		}
-		go httpServer.Serve(&oneConnListener{Listener: pln.ln, conn: c})
+		pln.ServeConn(ipp, c)
 	}
 }
 
+func (pln *peerAPIListener) ServeConn(src netaddr.IPPort, c net.Conn) {
+	logf := pln.lb.logf
+	peerNode, peerUser, ok := pln.lb.WhoIs(src)
+	if !ok {
+		logf("peerapi: unknown peer %v", src)
+		c.Close()
+		return
+	}
+	h := &peerAPIHandler{
+		ps:         pln.ps,
+		isSelf:     pln.ps.selfNode.User == peerNode.User,
+		remoteAddr: src,
+		peerNode:   peerNode,
+		peerUser:   peerUser,
+	}
+	httpServer := &http.Server{
+		Handler: h,
+	}
+	if addH2C != nil {
+		addH2C(httpServer)
+	}
+	go httpServer.Serve(&oneConnListener{Listener: pln.ln, conn: c})
+}
+
 type oneConnListener struct {
 	net.Listener
 	conn net.Conn
diff --git a/wgengine/netstack/netstack.go b/wgengine/netstack/netstack.go
index 72e1808ed..1501f4722 100644
--- a/wgengine/netstack/netstack.go
+++ b/wgengine/netstack/netstack.go
@@ -82,9 +82,12 @@ type Impl struct {
 	mc        *magicsock.Conn
 	logf      logger.Logf
 	dialer    *tsdial.Dialer
-	ctx       context.Context    // alive until Close
-	ctxCancel context.CancelFunc // called on Close
-	lb        *ipnlocal.LocalBackend
+	ctx       context.Context        // alive until Close
+	ctxCancel context.CancelFunc     // called on Close
+	lb        *ipnlocal.LocalBackend // or nil
+
+	peerapiPort4Atomic uint32 // uint16 port number for IPv4 peerapi
+	peerapiPort6Atomic uint32 // uint16 port number for IPv6 peerapi
 
 	// atomicIsLocalIPFunc holds a func that reports whether an IP
 	// is a local (non-subnet) Tailscale IP address of this
@@ -407,9 +410,33 @@ func (ns *Impl) processSSH() bool {
 	return ns.lb != nil && ns.lb.ShouldRunSSH()
 }
 
+func (ns *Impl) peerAPIPortAtomic(ip netaddr.IP) *uint32 {
+	if ip.Is4() {
+		return &ns.peerapiPort4Atomic
+	} else {
+		return &ns.peerapiPort6Atomic
+	}
+}
+
 // shouldProcessInbound reports whether an inbound packet should be
 // handled by netstack.
 func (ns *Impl) shouldProcessInbound(p *packet.Parsed, t *tstun.Wrapper) bool {
+	// Handle incoming peerapi connections in netstack.
+	if ns.lb != nil && p.IPProto == ipproto.TCP {
+		var peerAPIPort uint16
+		dstIP := p.Dst.IP()
+		if p.TCPFlags&packet.TCPSynAck == packet.TCPSyn && ns.isLocalIP(dstIP) {
+			if port, ok := ns.lb.GetPeerAPIPort(p.Dst.IP()); ok {
+				peerAPIPort = port
+				atomic.StoreUint32(ns.peerAPIPortAtomic(dstIP), uint32(port))
+			}
+		} else {
+			peerAPIPort = uint16(atomic.LoadUint32(ns.peerAPIPortAtomic(dstIP)))
+		}
+		if p.IPProto == ipproto.TCP && p.Dst.Port() == peerAPIPort {
+			return true
+		}
+	}
 	if ns.isInboundTSSH(p) && ns.processSSH() {
 		return true
 	}
@@ -621,6 +648,16 @@ func (ns *Impl) acceptTCP(r *tcp.ForwarderRequest) {
 		}
 		return
 	}
+	if ns.lb != nil {
+		if port, ok := ns.lb.GetPeerAPIPort(dialIP); ok {
+			if reqDetails.LocalPort == port && ns.isLocalIP(dialIP) {
+				src := netaddr.IPPortFrom(clientRemoteIP, reqDetails.RemotePort)
+				dst := netaddr.IPPortFrom(dialIP, port)
+				ns.lb.ServePeerAPIConnection(src, dst, c)
+				return
+			}
+		}
+	}
 	if ns.ForwardTCPIn != nil {
 		ns.ForwardTCPIn(c, reqDetails.LocalPort)
 		return