diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 8e561b3e0..40ab81447 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -3288,6 +3288,13 @@ func dnsConfigForNetmap(nm *netmap.NetworkMap, prefs ipn.PrefsView, logf logger.
 		return dcfg
 	}
 
+	// If we're using an exit node and that exit node is IsWireGuardOnly with
+	// ExitNodeDNSResolver set, then add that as the default.
+	if resolvers, ok := wireguardExitNodeDNSResolvers(nm, prefs.ExitNodeID()); ok {
+		addDefault(resolvers)
+		return dcfg
+	}
+
 	addDefault(nm.DNS.Resolvers)
 	for suffix, resolvers := range nm.DNS.Routes {
 		fqdn, err := dnsname.ToFQDN(suffix)
@@ -4676,6 +4683,30 @@ func exitNodeCanProxyDNS(nm *netmap.NetworkMap, exitNodeID tailcfg.StableNodeID)
 	return "", false
 }
 
+// wireguardExitNodeDNSResolvers returns the DNS resolvers to use for a
+// WireGuard-only exit node, if it has resolver addresses.
+func wireguardExitNodeDNSResolvers(nm *netmap.NetworkMap, exitNodeID tailcfg.StableNodeID) ([]*dnstype.Resolver, bool) {
+	if exitNodeID.IsZero() {
+		return nil, false
+	}
+
+	for _, p := range nm.Peers {
+		if p.StableID() == exitNodeID && p.IsWireGuardOnly() {
+			resolvers := p.ExitNodeDNSResolvers()
+			if !resolvers.IsNil() && resolvers.Len() > 0 {
+				copies := make([]*dnstype.Resolver, resolvers.Len())
+				for i := range resolvers.LenIter() {
+					copies[i] = resolvers.At(i).AsStruct()
+				}
+				return copies, true
+			}
+			return nil, false
+		}
+	}
+
+	return nil, false
+}
+
 func peerCanProxyDNS(p tailcfg.NodeView) bool {
 	if p.Cap() >= 26 {
 		// Actually added at 25
diff --git a/ipn/ipnlocal/local_test.go b/ipn/ipnlocal/local_test.go
index 6ad3a2b83..ad32a9757 100644
--- a/ipn/ipnlocal/local_test.go
+++ b/ipn/ipnlocal/local_test.go
@@ -22,6 +22,7 @@ import (
 	"tailscale.com/tailcfg"
 	"tailscale.com/tsd"
 	"tailscale.com/tstest"
+	"tailscale.com/types/dnstype"
 	"tailscale.com/types/key"
 	"tailscale.com/types/logger"
 	"tailscale.com/types/logid"
@@ -952,3 +953,109 @@ func TestUpdateNetmapDelta(t *testing.T) {
 		}
 	}
 }
+
+func TestWireguardExitNodeDNSResolvers(t *testing.T) {
+	type tc struct {
+		name          string
+		id            tailcfg.StableNodeID
+		peers         []*tailcfg.Node
+		wantOK        bool
+		wantResolvers []*dnstype.Resolver
+	}
+
+	tests := []tc{
+		{
+			name:          "no peers",
+			id:            "1",
+			wantOK:        false,
+			wantResolvers: nil,
+		},
+		{
+			name: "non wireguard peer",
+			id:   "1",
+			peers: []*tailcfg.Node{
+				{
+					StableID:             "1",
+					IsWireGuardOnly:      false,
+					ExitNodeDNSResolvers: []*dnstype.Resolver{{Addr: "dns.example.com"}},
+				},
+			},
+			wantOK:        false,
+			wantResolvers: nil,
+		},
+		{
+			name: "no matching IDs",
+			id:   "2",
+			peers: []*tailcfg.Node{
+				{
+					StableID:             "1",
+					IsWireGuardOnly:      true,
+					ExitNodeDNSResolvers: []*dnstype.Resolver{{Addr: "dns.example.com"}},
+				},
+			},
+			wantOK:        false,
+			wantResolvers: nil,
+		},
+		{
+			name: "wireguard peer",
+			id:   "1",
+			peers: []*tailcfg.Node{
+				{
+					StableID:             "1",
+					IsWireGuardOnly:      true,
+					ExitNodeDNSResolvers: []*dnstype.Resolver{{Addr: "dns.example.com"}},
+				},
+			},
+			wantOK:        true,
+			wantResolvers: []*dnstype.Resolver{{Addr: "dns.example.com"}},
+		},
+	}
+
+	for _, tc := range tests {
+		peers := nodeViews(tc.peers)
+		nm := &netmap.NetworkMap{
+			Peers: peers,
+		}
+		gotResolvers, gotOK := wireguardExitNodeDNSResolvers(nm, tc.id)
+
+		if gotOK != tc.wantOK || !resolversEqual(gotResolvers, tc.wantResolvers) {
+			t.Errorf("case: %s: got %v, %v, want %v, %v", tc.name, gotOK, gotResolvers, tc.wantOK, tc.wantResolvers)
+		}
+	}
+}
+
+func TestDNSConfigForNetmapForWireguardExitNode(t *testing.T) {
+	resolvers := []*dnstype.Resolver{{Addr: "dns.example.com"}}
+	nm := &netmap.NetworkMap{
+		Peers: nodeViews([]*tailcfg.Node{
+			{
+				StableID:             "1",
+				IsWireGuardOnly:      true,
+				ExitNodeDNSResolvers: resolvers,
+				Hostinfo:             (&tailcfg.Hostinfo{}).View(),
+			},
+		}),
+	}
+
+	prefs := &ipn.Prefs{
+		ExitNodeID: "1",
+		CorpDNS:    true,
+	}
+
+	got := dnsConfigForNetmap(nm, prefs.View(), t.Logf, "")
+	if !resolversEqual(got.DefaultResolvers, resolvers) {
+		t.Errorf("got %v, want %v", got.DefaultResolvers, resolvers)
+	}
+}
+
+func resolversEqual(a, b []*dnstype.Resolver) bool {
+	if len(a) != len(b) {
+		return false
+	}
+	for i := range a {
+		if !a[i].Equal(b[i]) {
+			return false
+		}
+	}
+	return true
+}