diff --git a/net/packet/tsmp.go b/net/packet/tsmp.go
index 8fad1d503..b9b805b1a 100644
--- a/net/packet/tsmp.go
+++ b/net/packet/tsmp.go
@@ -15,12 +15,10 @@ import (
 	"fmt"
 	"net/netip"
 
-	"go4.org/mem"
 	"tailscale.com/types/ipproto"
-	"tailscale.com/types/key"
 )
 
-const minTSMPSize = 7 // the rejected body is 7 bytes
+const minTSMPSize = 1 // minimum is 1 byte for the type field (e.g., disco key request 'd')
 
 // TailscaleRejectedHeader is a TSMP message that says that one
 // Tailscale node has rejected the connection from another. Unlike a
@@ -75,8 +73,11 @@ const (
 	// TSMPTypePong is the type byte for a TailscalePongResponse.
 	TSMPTypePong TSMPType = 'o'
 
-	// TSPMTypeDiscoAdvertisement is the type byte for sending disco keys
-	TSMPTypeDiscoAdvertisement TSMPType = 'a'
+	// TSMPTypeDiscoKeyRequest is the type byte for a disco key request.
+	TSMPTypeDiscoKeyRequest TSMPType = 'd'
+
+	// TSMPTypeDiscoKeyUpdate is the type byte for a disco key update.
+	TSMPTypeDiscoKeyUpdate TSMPType = 'D'
 )
 
 type TailscaleRejectReason byte
@@ -265,52 +266,62 @@ func (h TSMPPongReply) Marshal(buf []byte) error {
 	return nil
 }
 
-// TSMPDiscoKeyAdvertisement is a TSMP message that's used for distributing Disco Keys.
+// TSMPDiscoKeyRequest is a TSMP message that requests a peer's disco key.
 //
-// On the wire, after the IP header, it's currently 33 bytes:
-//   - 'a' (TSMPTypeDiscoAdvertisement)
-//   - 32 disco key bytes
-type TSMPDiscoKeyAdvertisement struct {
-	Src, Dst netip.Addr
-	Key      key.DiscoPublic
-}
+// On the wire, after the IP header, it's currently 1 byte:
+//   - 'd' (TSMPTypeDiscoKeyRequest)
+type TSMPDiscoKeyRequest struct{}
 
-func (ka *TSMPDiscoKeyAdvertisement) Marshal() ([]byte, error) {
-	var iph Header
-	if ka.Src.Is4() {
-		iph = IP4Header{
-			IPProto: ipproto.TSMP,
-			Src:     ka.Src,
-			Dst:     ka.Dst,
-		}
-	} else {
-		iph = IP6Header{
-			IPProto: ipproto.TSMP,
-			Src:     ka.Src,
-			Dst:     ka.Dst,
-		}
+func (pp *Parsed) AsTSMPDiscoKeyRequest() (h TSMPDiscoKeyRequest, ok bool) {
+	if pp.IPProto != ipproto.TSMP {
+		return
 	}
-	payload := make([]byte, 0, 33)
-	payload = append(payload, byte(TSMPTypeDiscoAdvertisement))
-	payload = ka.Key.AppendTo(payload)
-	if len(payload) != 33 {
-		// Mostly to safeguard against ourselves changing this in the future.
-		return []byte{}, fmt.Errorf("expected payload length 33, got %d", len(payload))
+	p := pp.Payload()
+	if len(p) < 1 || p[0] != byte(TSMPTypeDiscoKeyRequest) {
+		return
 	}
+	return h, true
+}
 
-	return Generate(iph, payload), nil
+// TSMPDiscoKeyUpdate is a TSMP message that contains a disco public key.
+// It may be sent in response to a request, or unsolicited when a node
+// believes its peer may have stale disco key information.
+//
+// On the wire, after the IP header, it's currently 33 bytes:
+//   - 'D' (TSMPTypeDiscoKeyUpdate)
+//   - 32 bytes disco public key
+type TSMPDiscoKeyUpdate struct {
+	IPHeader Header
+	DiscoKey [32]byte // raw disco public key bytes
 }
 
-func (pp *Parsed) AsTSMPDiscoAdvertisement() (tka TSMPDiscoKeyAdvertisement, ok bool) {
+// AsTSMPDiscoKeyUpdate returns pp as a TSMPDiscoKeyUpdate and whether it is one.
+// The update.IPHeader field is not populated.
+func (pp *Parsed) AsTSMPDiscoKeyUpdate() (update TSMPDiscoKeyUpdate, ok bool) {
 	if pp.IPProto != ipproto.TSMP {
 		return
 	}
 	p := pp.Payload()
-	if len(p) < 33 || p[0] != byte(TSMPTypeDiscoAdvertisement) {
+	if len(p) < 33 || p[0] != byte(TSMPTypeDiscoKeyUpdate) {
 		return
 	}
-	tka.Src = pp.Src.Addr()
-	tka.Key = key.DiscoPublicFromRaw32(mem.B(p[1:33]))
+	copy(update.DiscoKey[:], p[1:33])
+	return update, true
+}
 
-	return tka, true
+func (h TSMPDiscoKeyUpdate) Len() int {
+	return h.IPHeader.Len() + 33
+}
+
+func (h TSMPDiscoKeyUpdate) Marshal(buf []byte) error {
+	if len(buf) < h.Len() {
+		return errSmallBuffer
+	}
+	if err := h.IPHeader.Marshal(buf); err != nil {
+		return err
+	}
+	buf = buf[h.IPHeader.Len():]
+	buf[0] = byte(TSMPTypeDiscoKeyUpdate)
+	copy(buf[1:33], h.DiscoKey[:])
+	return nil
 }
diff --git a/net/packet/tsmp_test.go b/net/packet/tsmp_test.go
index d8f1d38d5..52e829d70 100644
--- a/net/packet/tsmp_test.go
+++ b/net/packet/tsmp_test.go
@@ -4,14 +4,8 @@
 package packet
 
 import (
-	"bytes"
-	"encoding/hex"
 	"net/netip"
-	"slices"
 	"testing"
-
-	"go4.org/mem"
-	"tailscale.com/types/key"
 )
 
 func TestTailscaleRejectedHeader(t *testing.T) {
@@ -78,61 +72,168 @@ func TestTailscaleRejectedHeader(t *testing.T) {
 	}
 }
 
-func TestTSMPDiscoKeyAdvertisementMarshal(t *testing.T) {
-	var (
-		// IPv4: Ver(4)Len(5), TOS, Len(53), ID, Flags, TTL(64), Proto(99), Cksum
-		headerV4, _ = hex.DecodeString("45000035000000004063705d")
-		// IPv6: Ver(6)TCFlow, Len(33), NextHdr(99), HopLim(64)
-		headerV6, _ = hex.DecodeString("6000000000216340")
-
-		packetType = []byte{'a'}
-		testKey    = bytes.Repeat([]byte{'a'}, 32)
-
-		// IPs
-		srcV4 = netip.MustParseAddr("1.2.3.4")
-		dstV4 = netip.MustParseAddr("4.3.2.1")
-		srcV6 = netip.MustParseAddr("2001:db8::1")
-		dstV6 = netip.MustParseAddr("2001:db8::2")
-	)
-
-	join := func(parts ...[]byte) []byte {
-		return bytes.Join(parts, nil)
+func TestTSMPDiscoKeyRequest(t *testing.T) {
+	t.Run("Manual", func(t *testing.T) {
+		var payload [1]byte
+		payload[0] = byte(TSMPTypeDiscoKeyRequest)
+
+		var p Parsed
+		p.IPProto = TSMP
+		p.dataofs = 40 // simulate after IP header
+		buf := make([]byte, 40+1)
+		copy(buf[40:], payload[:])
+		p.b = buf
+		p.length = len(buf)
+
+		_, ok := p.AsTSMPDiscoKeyRequest()
+		if !ok {
+			t.Fatal("failed to parse TSMP disco key request")
+		}
+	})
+
+	t.Run("RoundTripIPv4", func(t *testing.T) {
+		src := netip.MustParseAddr("100.64.0.1")
+		dst := netip.MustParseAddr("100.64.0.2")
+
+		iph := IP4Header{
+			IPProto: TSMP,
+			Src:     src,
+			Dst:     dst,
+		}
+
+		var payload [1]byte
+		payload[0] = byte(TSMPTypeDiscoKeyRequest)
+
+		pkt := Generate(iph, payload[:])
+		t.Logf("Generated packet: %d bytes, hex: %x", len(pkt), pkt)
+
+		// Manually check what decode4 would see
+		if len(pkt) >= 4 {
+			declaredLen := int(uint16(pkt[2])<<8 | uint16(pkt[3]))
+			t.Logf("Packet buffer length: %d, IP header declares length: %d", len(pkt), declaredLen)
+			t.Logf("Protocol byte at [9]: 0x%02x = %d", pkt[9], pkt[9])
+		}
+
+		var p Parsed
+		p.Decode(pkt)
+		t.Logf("Decoded: IPVersion=%d IPProto=%v Src=%v Dst=%v length=%d dataofs=%d",
+			p.IPVersion, p.IPProto, p.Src, p.Dst, p.length, p.dataofs)
+
+		if p.IPVersion != 4 {
+			t.Errorf("IPVersion = %d, want 4", p.IPVersion)
+		}
+		if p.IPProto != TSMP {
+			t.Errorf("IPProto = %v, want TSMP", p.IPProto)
+		}
+		if p.Src.Addr() != src {
+			t.Errorf("Src = %v, want %v", p.Src.Addr(), src)
+		}
+		if p.Dst.Addr() != dst {
+			t.Errorf("Dst = %v, want %v", p.Dst.Addr(), dst)
+		}
+
+		_, ok := p.AsTSMPDiscoKeyRequest()
+		if !ok {
+			t.Fatal("failed to parse TSMP disco key request from generated packet")
+		}
+	})
+
+	t.Run("RoundTripIPv6", func(t *testing.T) {
+		src := netip.MustParseAddr("2001:db8::1")
+		dst := netip.MustParseAddr("2001:db8::2")
+
+		iph := IP6Header{
+			IPProto: TSMP,
+			Src:     src,
+			Dst:     dst,
+		}
+
+		var payload [1]byte
+		payload[0] = byte(TSMPTypeDiscoKeyRequest)
+
+		pkt := Generate(iph, payload[:])
+		t.Logf("Generated packet: %d bytes", len(pkt))
+
+		var p Parsed
+		p.Decode(pkt)
+
+		if p.IPVersion != 6 {
+			t.Errorf("IPVersion = %d, want 6", p.IPVersion)
+		}
+		if p.IPProto != TSMP {
+			t.Errorf("IPProto = %v, want TSMP", p.IPProto)
+		}
+		if p.Src.Addr() != src {
+			t.Errorf("Src = %v, want %v", p.Src.Addr(), src)
+		}
+		if p.Dst.Addr() != dst {
+			t.Errorf("Dst = %v, want %v", p.Dst.Addr(), dst)
+		}
+
+		_, ok := p.AsTSMPDiscoKeyRequest()
+		if !ok {
+			t.Fatal("failed to parse TSMP disco key request from generated packet")
+		}
+	})
+}
+
+func TestTSMPDiscoKeyUpdate(t *testing.T) {
+	var discoKey [32]byte
+	for i := range discoKey {
+		discoKey[i] = byte(i + 10)
 	}
 
-	tests := []struct {
-		name string
-		tka  TSMPDiscoKeyAdvertisement
-		want []byte
-	}{
-		{
-			name: "v4Header",
-			tka: TSMPDiscoKeyAdvertisement{
-				Src: srcV4,
-				Dst: dstV4,
-				Key: key.DiscoPublicFromRaw32(mem.B(testKey)),
+	t.Run("IPv4", func(t *testing.T) {
+		update := TSMPDiscoKeyUpdate{
+			IPHeader: IP4Header{
+				IPProto: TSMP,
+				Src:     netip.MustParseAddr("1.2.3.4"),
+				Dst:     netip.MustParseAddr("5.6.7.8"),
 			},
-			want: join(headerV4, srcV4.AsSlice(), dstV4.AsSlice(), packetType, testKey),
-		},
-		{
-			name: "v6Header",
-			tka: TSMPDiscoKeyAdvertisement{
-				Src: srcV6,
-				Dst: dstV6,
-				Key: key.DiscoPublicFromRaw32(mem.B(testKey)),
+			DiscoKey: discoKey,
+		}
+
+		pkt := make([]byte, update.Len())
+		if err := update.Marshal(pkt); err != nil {
+			t.Fatal(err)
+		}
+
+		var p Parsed
+		p.Decode(pkt)
+
+		parsed, ok := p.AsTSMPDiscoKeyUpdate()
+		if !ok {
+			t.Fatal("failed to parse TSMP disco key update")
+		}
+		if parsed.DiscoKey != discoKey {
+			t.Errorf("disco key mismatch: got %v, want %v", parsed.DiscoKey, discoKey)
+		}
+	})
+
+	t.Run("IPv6", func(t *testing.T) {
+		update := TSMPDiscoKeyUpdate{
+			IPHeader: IP6Header{
+				IPProto: TSMP,
+				Src:     netip.MustParseAddr("2001:db8::1"),
+				Dst:     netip.MustParseAddr("2001:db8::2"),
 			},
-			want: join(headerV6, srcV6.AsSlice(), dstV6.AsSlice(), packetType, testKey),
-		},
-	}
+			DiscoKey: discoKey,
+		}
 
-	for _, tt := range tests {
-		t.Run(tt.name, func(t *testing.T) {
-			got, err := tt.tka.Marshal()
-			if err != nil {
-				t.Errorf("error mashalling TSMPDiscoAdvertisement: %s", err)
-			}
-			if !slices.Equal(got, tt.want) {
-				t.Errorf("error mashalling TSMPDiscoAdvertisement, expected: \n%x, \ngot:\n%x", tt.want, got)
-			}
-		})
-	}
+		pkt := make([]byte, update.Len())
+		if err := update.Marshal(pkt); err != nil {
+			t.Fatal(err)
+		}
+
+		var p Parsed
+		p.Decode(pkt)
+
+		parsed, ok := p.AsTSMPDiscoKeyUpdate()
+		if !ok {
+			t.Fatal("failed to parse TSMP disco key update")
+		}
+		if parsed.DiscoKey != discoKey {
+			t.Errorf("disco key mismatch: got %v, want %v", parsed.DiscoKey, discoKey)
+		}
+	})
 }
diff --git a/net/tstun/wrap.go b/net/tstun/wrap.go
index 6e07c7a3d..0619276ae 100644
--- a/net/tstun/wrap.go
+++ b/net/tstun/wrap.go
@@ -194,6 +194,10 @@ type Wrapper struct {
 	// false otherwise.
 	OnICMPEchoResponseReceived func(*packet.Parsed) bool
 
+	// GetDiscoPublicKey, if non-nil, returns the local node's disco public key.
+	// This is called when responding to TSMP disco key requests.
+	GetDiscoPublicKey func() key.DiscoPublic
+
 	// PeerAPIPort, if non-nil, returns the peerapi port that's
 	// running for the given IP address.
 	PeerAPIPort func(netip.Addr) (port uint16, ok bool)
@@ -211,8 +215,8 @@ type Wrapper struct {
 
 	metrics *metrics
 
-	eventClient              *eventbus.Client
-	discoKeyAdvertisementPub *eventbus.Publisher[DiscoKeyAdvertisement]
+	eventClient       *eventbus.Client
+	discoKeyUpdatePub *eventbus.Publisher[DiscoKeyUpdate]
 }
 
 type metrics struct {
@@ -227,6 +231,12 @@ func registerMetrics(reg *usermetric.Registry) *metrics {
 	}
 }
 
+// DiscoKeyUpdate is published on the event bus when a TSMP disco key update is received.
+type DiscoKeyUpdate struct {
+	SrcIP netip.Addr
+	Key   [32]byte
+}
+
 // tunInjectedRead is an injected packet pretending to be a tun.Read().
 type tunInjectedRead struct {
 	// Only one of packet or data should be set, and are read in that order of
@@ -288,7 +298,7 @@ func wrap(logf logger.Logf, tdev tun.Device, isTAP bool, m *usermetric.Registry,
 	}
 
 	w.eventClient = bus.Client("net.tstun")
-	w.discoKeyAdvertisementPub = eventbus.Publish[DiscoKeyAdvertisement](w.eventClient)
+	w.discoKeyUpdatePub = eventbus.Publish[DiscoKeyUpdate](w.eventClient)
 
 	w.vectorBuffer = make([][]byte, tdev.BatchSize())
 	for i := range w.vectorBuffer {
@@ -1126,11 +1136,6 @@ func (t *Wrapper) injectedRead(res tunInjectedRead, outBuffs [][]byte, sizes []i
 	return n, err
 }
 
-type DiscoKeyAdvertisement struct {
-	Src netip.Addr
-	Key key.DiscoPublic
-}
-
 func (t *Wrapper) filterPacketInboundFromWireGuard(p *packet.Parsed, captHook packet.CaptureCallback, pc *peerConfigTable, gro *gro.GRO) (filter.Response, *gro.GRO) {
 	if captHook != nil {
 		captHook(packet.FromPeer, t.now(), p.Buffer(), p.CaptureMeta)
@@ -1141,16 +1146,21 @@ func (t *Wrapper) filterPacketInboundFromWireGuard(p *packet.Parsed, captHook pa
 			t.noteActivity()
 			t.injectOutboundPong(p, pingReq)
 			return filter.DropSilently, gro
-		} else if discoKeyAdvert, ok := p.AsTSMPDiscoAdvertisement(); ok {
-			t.discoKeyAdvertisementPub.Publish(DiscoKeyAdvertisement{
-				Src: discoKeyAdvert.Src,
-				Key: discoKeyAdvert.Key,
-			})
-			return filter.DropSilently, gro
 		} else if data, ok := p.AsTSMPPong(); ok {
 			if f := t.OnTSMPPongReceived; f != nil {
 				f(data)
 			}
+		} else if _, ok := p.AsTSMPDiscoKeyRequest(); ok {
+			t.noteActivity()
+			t.injectOutboundDiscoKeyUpdate(p)
+			return filter.DropSilently, gro
+		} else if discoKeyUpdate, ok := p.AsTSMPDiscoKeyUpdate(); ok {
+			// Publish to eventbus for subscribers
+			t.discoKeyUpdatePub.Publish(DiscoKeyUpdate{
+				SrcIP: p.Src.Addr(),
+				Key:   discoKeyUpdate.DiscoKey,
+			})
+			return filter.DropSilently, gro
 		}
 	}
 
@@ -1459,6 +1469,36 @@ func (t *Wrapper) injectOutboundPong(pp *packet.Parsed, req packet.TSMPPingReque
 	t.InjectOutbound(packet.Generate(pong, nil))
 }
 
+func (t *Wrapper) injectOutboundDiscoKeyUpdate(pp *packet.Parsed) {
+	if t.GetDiscoPublicKey == nil {
+		return
+	}
+
+	discoKey := t.GetDiscoPublicKey()
+	if discoKey.IsZero() {
+		return
+	}
+
+	update := packet.TSMPDiscoKeyUpdate{
+		DiscoKey: discoKey.Raw32(),
+	}
+
+	switch pp.IPVersion {
+	case 4:
+		h4 := pp.IP4Header()
+		h4.ToResponse()
+		update.IPHeader = h4
+	case 6:
+		h6 := pp.IP6Header()
+		h6.ToResponse()
+		update.IPHeader = h6
+	default:
+		return
+	}
+
+	t.InjectOutbound(packet.Generate(update, nil))
+}
+
 // InjectOutbound makes the Wrapper device behave as if a packet
 // with the given contents was sent to the network.
 // It does not block, but takes ownership of the packet.
diff --git a/net/tstun/wrap_test.go b/net/tstun/wrap_test.go
index c7d0708df..2d33228b8 100644
--- a/net/tstun/wrap_test.go
+++ b/net/tstun/wrap_test.go
@@ -966,28 +966,57 @@ func TestCaptureHook(t *testing.T) {
 }
 
 func TestTSMPDisco(t *testing.T) {
-	t.Run("IPv6DiscoAdvert", func(t *testing.T) {
+	t.Run("DiscoKeyRequest", func(t *testing.T) {
 		src := netip.MustParseAddr("2001:db8::1")
 		dst := netip.MustParseAddr("2001:db8::2")
-		discoKey := key.NewDisco()
-		buf, _ := (&packet.TSMPDiscoKeyAdvertisement{
-			Src: src,
-			Dst: dst,
-			Key: discoKey.Public(),
-		}).Marshal()
+
+		iph := packet.IP6Header{
+			IPProto: ipproto.TSMP,
+			Src:     src,
+			Dst:     dst,
+		}
+
+		var payload [1]byte
+		payload[0] = byte(packet.TSMPTypeDiscoKeyRequest)
+		buf := packet.Generate(iph, payload[:])
 
 		var p packet.Parsed
 		p.Decode(buf)
 
-		tda, ok := p.AsTSMPDiscoAdvertisement()
+		_, ok := p.AsTSMPDiscoKeyRequest()
 		if !ok {
-			t.Error("Unable to parse message as TSMPDiscoAdversitement")
+			t.Error("Unable to parse message as TSMPDiscoKeyRequest")
 		}
-		if tda.Src != src {
-			t.Errorf("Src address did not match, expected %v, got %v", src, tda.Src)
+	})
+
+	t.Run("DiscoKeyUpdate", func(t *testing.T) {
+		src := netip.MustParseAddr("2001:db8::1")
+		dst := netip.MustParseAddr("2001:db8::2")
+		discoKey := key.NewDisco()
+
+		update := packet.TSMPDiscoKeyUpdate{
+			IPHeader: packet.IP6Header{
+				IPProto: ipproto.TSMP,
+				Src:     src,
+				Dst:     dst,
+			},
+			DiscoKey: discoKey.Public().Raw32(),
+		}
+
+		buf := make([]byte, update.Len())
+		if err := update.Marshal(buf); err != nil {
+			t.Fatal(err)
+		}
+
+		var p packet.Parsed
+		p.Decode(buf)
+
+		parsed, ok := p.AsTSMPDiscoKeyUpdate()
+		if !ok {
+			t.Error("Unable to parse message as TSMPDiscoKeyUpdate")
 		}
-		if !reflect.DeepEqual(tda.Key, discoKey.Public()) {
-			t.Errorf("Key did not match, expected %q, got %q", discoKey.Public(), tda.Key)
+		if parsed.DiscoKey != discoKey.Public().Raw32() {
+			t.Errorf("Key did not match, expected %v, got %v", discoKey.Public().Raw32(), parsed.DiscoKey)
 		}
 	})
 }
diff --git a/wgengine/magicsock/derp.go b/wgengine/magicsock/derp.go
index 37a4f1a64..e20acadc4 100644
--- a/wgengine/magicsock/derp.go
+++ b/wgengine/magicsock/derp.go
@@ -721,6 +721,16 @@ func (c *Conn) processDERPReadResult(dm derpReadResult, b []byte) (n int, ep *en
 		update(0, netip.AddrPortFrom(ep.nodeAddr, 0), srcAddr.ap, 1, dm.n, true)
 	}
 
+	// Request disco key from peer via TSMP if we receive a WireGuard handshake
+	// over DERP without recent disco success. This handles the "WireGuard-first"
+	// case where WireGuard establishes a tunnel via DERP before disco succeeds
+	// (e.g., control plane unreachable or stale disco keys).
+	if looksLikeWireGuardHandshake(b[:n]) && n > 0 {
+		c.mu.Lock()
+		c.requestDiscoKeyViaTSMPLocked(dm.src, ep)
+		c.mu.Unlock()
+	}
+
 	c.metrics.inboundPacketsDERPTotal.Add(1)
 	c.metrics.inboundBytesDERPTotal.Add(int64(n))
 	return n, ep
diff --git a/wgengine/magicsock/magicsock.go b/wgengine/magicsock/magicsock.go
index 064838a2d..da4f5c47d 100644
--- a/wgengine/magicsock/magicsock.go
+++ b/wgengine/magicsock/magicsock.go
@@ -178,9 +178,10 @@ type Conn struct {
 
 	// A publisher for synchronization points to ensure correct ordering of
 	// config changes between magicsock and wireguard.
-	syncPub               *eventbus.Publisher[syncPoint]
-	allocRelayEndpointPub *eventbus.Publisher[UDPRelayAllocReq]
-	portUpdatePub         *eventbus.Publisher[router.PortUpdate]
+	syncPub                *eventbus.Publisher[syncPoint]
+	allocRelayEndpointPub  *eventbus.Publisher[UDPRelayAllocReq]
+	portUpdatePub          *eventbus.Publisher[router.PortUpdate]
+	tsmpDiscoKeyRequestPub *eventbus.Publisher[TSMPDiscoKeyRequest]
 
 	// pconn4 and pconn6 are the underlying UDP sockets used to
 	// send/receive packets for wireguard and other magicsock
@@ -572,6 +573,14 @@ type UDPRelayAllocReq struct {
 	Message *disco.AllocateUDPRelayEndpointRequest
 }
 
+// TSMPDiscoKeyRequest is published on the event bus when magicsock needs to
+// send a TSMP disco key request to a peer. Subscribers should inject the
+// TSMP packet into the tunnel device.
+type TSMPDiscoKeyRequest struct {
+	DstIP      netip.Addr
+	MetricSent *clientmetric.Metric
+}
+
 // UDPRelayAllocResp represents a [*disco.AllocateUDPRelayEndpointResponse]
 // that is yet to be transmitted over DERP (or delivered locally if
 // ReqRxFromNodeKey is self). This is signaled over an [eventbus.Bus] from
@@ -691,6 +700,7 @@ func NewConn(opts Options) (*Conn, error) {
 	c.syncPub = eventbus.Publish[syncPoint](ec)
 	c.allocRelayEndpointPub = eventbus.Publish[UDPRelayAllocReq](ec)
 	c.portUpdatePub = eventbus.Publish[router.PortUpdate](ec)
+	c.tsmpDiscoKeyRequestPub = eventbus.Publish[TSMPDiscoKeyRequest](ec)
 	eventbus.SubscribeFunc(ec, c.onPortMapChanged)
 	eventbus.SubscribeFunc(ec, c.onFilterUpdate)
 	eventbus.SubscribeFunc(ec, c.onNodeViewsUpdate)
@@ -1800,6 +1810,15 @@ func looksLikeInitiationMsg(b []byte) bool {
 		binary.LittleEndian.Uint32(b) == device.MessageInitiationType
 }
 
+func looksLikeWireGuardHandshake(b []byte) bool {
+	if len(b) < 4 {
+		return false
+	}
+	msgType := binary.LittleEndian.Uint32(b)
+	return (len(b) == device.MessageInitiationSize && msgType == device.MessageInitiationType) ||
+		(len(b) == device.MessageResponseSize && msgType == device.MessageResponseType)
+}
+
 // receiveIP is the shared bits of ReceiveIPv4 and ReceiveIPv6.
 //
 // size is the length of 'b' to report up to wireguard-go (only relevant if
@@ -4104,6 +4123,12 @@ var (
 	metricUDPLifetimeCycleCompleteAt10sCliff     = newUDPLifetimeCounter("magicsock_udp_lifetime_cycle_complete_at_10s_cliff")
 	metricUDPLifetimeCycleCompleteAt30sCliff     = newUDPLifetimeCounter("magicsock_udp_lifetime_cycle_complete_at_30s_cliff")
 	metricUDPLifetimeCycleCompleteAt60sCliff     = newUDPLifetimeCounter("magicsock_udp_lifetime_cycle_complete_at_60s_cliff")
+
+	// TSMP disco key exchange
+	metricTSMPDiscoKeyRequestSent    = clientmetric.NewCounter("magicsock_tsmp_disco_key_request_sent")
+	metricTSMPDiscoKeyUpdateReceived = clientmetric.NewCounter("magicsock_tsmp_disco_key_update_received")
+	metricTSMPDiscoKeyUpdateApplied  = clientmetric.NewCounter("magicsock_tsmp_disco_key_update_applied")
+	metricTSMPDiscoKeyUpdateUnknown  = clientmetric.NewCounter("magicsock_tsmp_disco_key_update_unknown_peer")
 )
 
 // newUDPLifetimeCounter returns a new *clientmetric.Metric with the provided
@@ -4242,6 +4267,81 @@ func (le *lazyEndpoint) FromPeer(peerPublicKey [32]byte) {
 	//  See http://go/corp/29422 & http://go/corp/30042
 	le.c.peerMap.setNodeKeyForEpAddr(le.src, pubKey)
 	le.c.logf("magicsock: lazyEndpoint.FromPeer(%v) setting epAddr(%v) in peerMap for node(%v)", pubKey.ShortString(), le.src, ep.nodeAddr)
+
+	le.c.requestDiscoKeyViaTSMPLocked(pubKey, ep)
+}
+
+// requestDiscoKeyViaTSMPLocked sends a TSMP disco key request to a peer if there
+// hasn't been a recent disco ping.
+// c.mu must be held.
+func (c *Conn) requestDiscoKeyViaTSMPLocked(nodeKey key.NodePublic, ep *endpoint) {
+	if !ep.nodeAddr.IsValid() {
+		return
+	}
+
+	epDisco := ep.disco.Load()
+	if epDisco != nil {
+		di := c.discoInfo[epDisco.key]
+		recentDiscoPing := di != nil && time.Since(di.lastPingTime) < discoPingInterval
+
+		if recentDiscoPing {
+			return
+		}
+	}
+
+	go c.tsmpDiscoKeyRequestPub.Publish(TSMPDiscoKeyRequest{DstIP: ep.nodeAddr, MetricSent: metricTSMPDiscoKeyRequestSent})
+}
+
+// HandleDiscoKeyUpdate processes a TSMP disco key update.
+// The update may be solicited (in response to a request) or unsolicited.
+// srcIP is the Tailscale IP of the peer that sent the update.
+func (c *Conn) HandleDiscoKeyUpdate(srcIP netip.Addr, update packet.TSMPDiscoKeyUpdate) {
+	discoKey := key.DiscoPublicFromRaw32(mem.B(update.DiscoKey[:]))
+	c.logf("magicsock: received disco key update %v from %v", discoKey.ShortString(), srcIP)
+	metricTSMPDiscoKeyUpdateReceived.Add(1)
+
+	c.mu.Lock()
+	defer c.mu.Unlock()
+
+	var nodeKey key.NodePublic
+	var found bool
+	for _, peer := range c.peers.All() {
+		for _, addr := range peer.Addresses().All() {
+			if addr.Addr() == srcIP {
+				nodeKey = peer.Key()
+				found = true
+				break
+			}
+		}
+		if found {
+			break
+		}
+	}
+
+	if !found {
+		c.logf("magicsock: disco key update from unknown peer %v", srcIP)
+		metricTSMPDiscoKeyUpdateUnknown.Add(1)
+		return
+	}
+
+	ep, ok := c.peerMap.endpointForNodeKey(nodeKey)
+	if !ok {
+		c.logf("magicsock: endpoint not found for node %v", nodeKey.ShortString())
+		return
+	}
+
+	oldDiscoKey := key.DiscoPublic{}
+	if epDisco := ep.disco.Load(); epDisco != nil {
+		oldDiscoKey = epDisco.key
+	}
+	c.discoInfoForKnownPeerLocked(discoKey)
+	ep.disco.Store(&endpointDisco{
+		key:   discoKey,
+		short: discoKey.ShortString(),
+	})
+	c.peerMap.upsertEndpoint(ep, oldDiscoKey)
+	c.logf("magicsock: updated disco key for peer %v to %v", nodeKey.ShortString(), discoKey.ShortString())
+	metricTSMPDiscoKeyUpdateApplied.Add(1)
 }
 
 // PeerRelays returns the current set of candidate peer relays.
diff --git a/wgengine/magicsock/magicsock_test.go b/wgengine/magicsock/magicsock_test.go
index 4e1024886..b7694ba56 100644
--- a/wgengine/magicsock/magicsock_test.go
+++ b/wgengine/magicsock/magicsock_test.go
@@ -64,6 +64,7 @@ import (
 	"tailscale.com/types/netmap"
 	"tailscale.com/types/nettype"
 	"tailscale.com/types/ptr"
+	"tailscale.com/types/views"
 	"tailscale.com/util/cibuild"
 	"tailscale.com/util/clientmetric"
 	"tailscale.com/util/eventbus"
@@ -4302,3 +4303,66 @@ func TestRotateDiscoKeyMultipleTimes(t *testing.T) {
 		keys = append(keys, newKey)
 	}
 }
+
+func TestSendTSMPDiscoKeyRequest(t *testing.T) {
+	ep := &endpoint{
+		nodeID:    1,
+		publicKey: key.NewNode().Public(),
+		nodeAddr:  netip.MustParseAddr("100.64.0.1"),
+	}
+	discoKey := key.NewDisco().Public()
+	ep.disco.Store(&endpointDisco{
+		key:   discoKey,
+		short: discoKey.ShortString(),
+	})
+	bus := eventbustest.NewBus(t)
+	conn := newConn(t.Logf)
+	conn.eventBus = bus
+	conn.eventClient = bus.Client("magicsock.Conn.test")
+	conn.tsmpDiscoKeyRequestPub = eventbus.Publish[TSMPDiscoKeyRequest](conn.eventClient)
+	ep.c = conn
+
+	tsmpRequestCalled := make(chan struct{}, 1)
+	var capturedIP netip.Addr
+	ec := bus.Client("test")
+	defer ec.Close()
+	eventbus.SubscribeFunc(ec, func(req TSMPDiscoKeyRequest) {
+		capturedIP = req.DstIP
+		if req.MetricSent != nil {
+			req.MetricSent.Add(1)
+		}
+		tsmpRequestCalled <- struct{}{}
+	})
+
+	conn.mu.Lock()
+	conn.peers = views.SliceOf([]tailcfg.NodeView{
+		(&tailcfg.Node{
+			Key: ep.publicKey,
+			Addresses: []netip.Prefix{
+				netip.MustParsePrefix("100.64.0.1/32"),
+			},
+		}).View(),
+	})
+	conn.mu.Unlock()
+
+	var pubKey [32]byte
+	copy(pubKey[:], ep.publicKey.AppendTo(nil))
+	conn.peerMap.upsertEndpoint(ep, key.DiscoPublic{})
+
+	le := &lazyEndpoint{
+		c:   conn,
+		src: epAddr{ap: netip.MustParseAddrPort("127.0.0.1:7777")},
+	}
+
+	le.FromPeer(pubKey)
+
+	select {
+	case <-tsmpRequestCalled:
+		if !capturedIP.IsValid() {
+			t.Error("TSMP request sent with invalid IP")
+		}
+		t.Logf("TSMP disco key request sent to %v", capturedIP)
+	case <-time.After(time.Second):
+		t.Error("TSMP disco key request was not sent")
+	}
+}
diff --git a/wgengine/userspace.go b/wgengine/userspace.go
index a369fa343..c0e79633a 100644
--- a/wgengine/userspace.go
+++ b/wgengine/userspace.go
@@ -54,6 +54,7 @@ import (
 	"tailscale.com/util/execqueue"
 	"tailscale.com/util/mak"
 	"tailscale.com/util/set"
+	"tailscale.com/util/singleflight"
 	"tailscale.com/util/testenv"
 	"tailscale.com/util/usermetric"
 	"tailscale.com/version"
@@ -469,6 +470,13 @@ func NewUserspaceEngine(logf logger.Logf, conf Config) (_ Engine, reterr error)
 		return true
 	}
 
+	e.tundev.GetDiscoPublicKey = func() key.DiscoPublic {
+		if e.magicConn == nil {
+			return key.DiscoPublic{}
+		}
+		return e.magicConn.DiscoPublicKey()
+	}
+
 	// wgdev takes ownership of tundev, will close it when closed.
 	e.logf("Creating WireGuard device...")
 	e.wgdev = wgcfg.NewDevice(e.tundev, e.magicConn.Bind(), e.wgLogger.DeviceLogger)
@@ -549,6 +557,36 @@ func NewUserspaceEngine(logf logger.Logf, conf Config) (_ Engine, reterr error)
 		}
 		e.linkChangeQueue.Add(func() { e.linkChange(&cd) })
 	})
+	eventbus.SubscribeFunc(ec, func(update tstun.DiscoKeyUpdate) {
+		e.logf("wgengine: got TSMP disco key update from %v via eventbus", update.SrcIP)
+		if e.magicConn != nil {
+			pkt := packet.TSMPDiscoKeyUpdate{
+				DiscoKey: update.Key,
+			}
+			e.magicConn.HandleDiscoKeyUpdate(update.SrcIP, pkt)
+		}
+	})
+	var tsmpRequestGroup singleflight.Group[netip.Addr, struct{}]
+	eventbus.SubscribeFunc(ec, func(req magicsock.TSMPDiscoKeyRequest) {
+		go tsmpRequestGroup.Do(req.DstIP, func() (struct{}, error) {
+			// DiscoKeyRequests are triggered by an incoming WireGuard handshake
+			// initiation arriving before a disco ping, which is a likely
+			// indicator that disco pings failed due to a lack of key
+			// synchronization. If the requests are sent immediately, before the
+			// handshake state is accepted in the WireGuard client state
+			// machine, this starts a new session, and the two peer state
+			// machines conflict, causing loss and additional delays. Delaying
+			// the send avoids this, so coalesce duplicate sends, and delay them
+			// by a short time to avoid the state machine conflict.
+			time.Sleep(time.Millisecond)
+			if err := e.sendTSMPDiscoKeyRequest(req.DstIP); err != nil {
+				e.logf("wgengine: failed to send TSMP disco key request: %v", err)
+			}
+			e.logf("wgengine: sending TSMP disco key request to %v", req.DstIP)
+			req.MetricSent.Add(1)
+			return struct{}{}, nil
+		})
+	})
 	e.eventClient = ec
 	e.logf("Engine created.")
 	return e, nil
@@ -1436,7 +1474,6 @@ func (e *userspaceEngine) Ping(ip netip.Addr, pingType tailcfg.PingType, size in
 		e.magicConn.Ping(peer, res, size, cb)
 	case "TSMP":
 		e.sendTSMPPing(ip, peer, res, cb)
-		e.sendTSMPDiscoAdvertisement(ip)
 	case "ICMP":
 		e.sendICMPEchoRequest(ip, peer, res, cb)
 	}
@@ -1557,29 +1594,6 @@ func (e *userspaceEngine) sendTSMPPing(ip netip.Addr, peer tailcfg.NodeView, res
 	e.tundev.InjectOutbound(tsmpPing)
 }
 
-func (e *userspaceEngine) sendTSMPDiscoAdvertisement(ip netip.Addr) {
-	srcIP, err := e.mySelfIPMatchingFamily(ip)
-	if err != nil {
-		e.logf("getting matching node: %s", err)
-		return
-	}
-	tdka := packet.TSMPDiscoKeyAdvertisement{
-		Src: srcIP,
-		Dst: ip,
-		Key: e.magicConn.DiscoPublicKey(),
-	}
-	payload, err := tdka.Marshal()
-	if err != nil {
-		e.logf("error generating TSMP Advertisement: %s", err)
-		metricTSMPDiscoKeyAdvertisementError.Add(1)
-	} else if err := e.tundev.InjectOutbound(payload); err != nil {
-		e.logf("error sending TSMP Advertisement: %s", err)
-		metricTSMPDiscoKeyAdvertisementError.Add(1)
-	} else {
-		metricTSMPDiscoKeyAdvertisementSent.Add(1)
-	}
-}
-
 func (e *userspaceEngine) setTSMPPongCallback(data [8]byte, cb func(packet.TSMPPongReply)) {
 	e.mu.Lock()
 	defer e.mu.Unlock()
@@ -1593,6 +1607,35 @@ func (e *userspaceEngine) setTSMPPongCallback(data [8]byte, cb func(packet.TSMPP
 	}
 }
 
+// sendTSMPDiscoKeyRequest sends a TSMP disco key request to the given peer IP.
+func (e *userspaceEngine) sendTSMPDiscoKeyRequest(ip netip.Addr) error {
+	srcIP, err := e.mySelfIPMatchingFamily(ip)
+	if err != nil {
+		return err
+	}
+
+	var iph packet.Header
+	if srcIP.Is4() {
+		iph = packet.IP4Header{
+			IPProto: ipproto.TSMP,
+			Src:     srcIP,
+			Dst:     ip,
+		}
+	} else {
+		iph = packet.IP6Header{
+			IPProto: ipproto.TSMP,
+			Src:     srcIP,
+			Dst:     ip,
+		}
+	}
+
+	var tsmpPayload [1]byte
+	tsmpPayload[0] = byte(packet.TSMPTypeDiscoKeyRequest)
+
+	tsmpRequest := packet.Generate(iph, tsmpPayload[:])
+	return e.tundev.InjectOutbound(tsmpRequest)
+}
+
 func (e *userspaceEngine) setICMPEchoResponseCallback(idSeq uint32, cb func()) {
 	e.mu.Lock()
 	defer e.mu.Unlock()
@@ -1746,9 +1789,6 @@ var (
 
 	metricNumMajorChanges = clientmetric.NewCounter("wgengine_major_changes")
 	metricNumMinorChanges = clientmetric.NewCounter("wgengine_minor_changes")
-
-	metricTSMPDiscoKeyAdvertisementSent  = clientmetric.NewCounter("magicsock_tsmp_disco_key_advertisement_sent")
-	metricTSMPDiscoKeyAdvertisementError = clientmetric.NewCounter("magicsock_tsmp_disco_key_advertisement_error")
 )
 
 func (e *userspaceEngine) InstallCaptureHook(cb packet.CaptureCallback) {
diff --git a/wgengine/userspace_test.go b/wgengine/userspace_test.go
index 0a1d2924d..abcf2f64f 100644
--- a/wgengine/userspace_test.go
+++ b/wgengine/userspace_test.go
@@ -325,7 +325,7 @@ func TestUserspaceEnginePeerMTUReconfig(t *testing.T) {
 	}
 }
 
-func TestTSMPKeyAdvertisement(t *testing.T) {
+func TestTSMPDiscoKeyRequest(t *testing.T) {
 	var knobs controlknobs.Knobs
 
 	bus := eventbustest.NewBus(t)
@@ -369,13 +369,12 @@ func TestTSMPKeyAdvertisement(t *testing.T) {
 		t.Fatal(err)
 	}
 
-	addr := netip.MustParseAddr("100.100.99.1")
-	previousValue := metricTSMPDiscoKeyAdvertisementSent.Value()
-	ue.sendTSMPDiscoAdvertisement(addr)
-	if val := metricTSMPDiscoKeyAdvertisementSent.Value(); val <= previousValue {
-		errs := metricTSMPDiscoKeyAdvertisementError.Value()
-		t.Errorf("Expected 1 disco key advert, got %d, errors %d", val, errs)
+	peerAddr := netip.MustParseAddr("100.100.99.1")
+	err = ue.sendTSMPDiscoKeyRequest(peerAddr)
+	if err != nil {
+		t.Fatalf("sendTSMPDiscoKeyRequest failed: %v", err)
 	}
+
 	// Remove config to have the engine shut down more consistently
 	err = ue.Reconfig(&wgcfg.Config{}, &router.Config{}, &dns.Config{})
 	if err != nil {