diff --git a/cmd/tailscaled/depaware.txt b/cmd/tailscaled/depaware.txt
index 56a755ec6..3b7cb2e36 100644
--- a/cmd/tailscaled/depaware.txt
+++ b/cmd/tailscaled/depaware.txt
@@ -89,7 +89,7 @@ tailscale.com/cmd/tailscaled dependencies: (generated by github.com/tailscale/de
   LW 💣 github.com/digitalocean/go-smbios/smbios                     from tailscale.com/posture
      💣 github.com/djherbis/times                                    from tailscale.com/drive/driveimpl
         github.com/fxamacker/cbor/v2                                 from tailscale.com/tka
-        github.com/gaissmai/bart                                     from tailscale.com/net/tstun
+        github.com/gaissmai/bart                                     from tailscale.com/net/tstun+
         github.com/go-json-experiment/json/internal                  from github.com/go-json-experiment/json/internal/jsonflags+
         github.com/go-json-experiment/json/internal/jsonflags        from github.com/go-json-experiment/json/internal/jsonopts+
         github.com/go-json-experiment/json/internal/jsonopts         from github.com/go-json-experiment/json/jsontext
diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 84f18fe01..6cb5855ce 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -3590,6 +3590,7 @@ func (b *LocalBackend) authReconfig() {
 	nm := b.netMap
 	hasPAC := b.prevIfState.HasPAC()
 	disableSubnetsIfPAC := nm.HasCap(tailcfg.NodeAttrDisableSubnetsIfPAC)
+	userDialUseRoutes := nm.HasCap(tailcfg.NodeAttrUserDialUseRoutes)
 	dohURL, dohURLOK := exitNodeCanProxyDNS(nm, b.peers, prefs.ExitNodeID())
 	dcfg := dnsConfigForNetmap(nm, b.peers, prefs, b.logf, version.OS())
 	// If the current node is an app connector, ensure the app connector machine is started
@@ -3647,6 +3648,12 @@ func (b *LocalBackend) authReconfig() {
 	}
 	b.logf("[v1] authReconfig: ra=%v dns=%v 0x%02x: %v", prefs.RouteAll(), prefs.CorpDNS(), flags, err)
 
+	if userDialUseRoutes {
+		b.dialer.SetRoutes(rcfg.Routes, rcfg.LocalRoutes)
+	} else {
+		b.dialer.SetRoutes(nil, nil)
+	}
+
 	b.initPeerAPIListener()
 }
 
diff --git a/net/tsdial/tsdial.go b/net/tsdial/tsdial.go
index 80d208f4f..42433b871 100644
--- a/net/tsdial/tsdial.go
+++ b/net/tsdial/tsdial.go
@@ -14,9 +14,11 @@
 	"runtime"
 	"strings"
 	"sync"
+	"sync/atomic"
 	"syscall"
 	"time"
 
+	"github.com/gaissmai/bart"
 	"tailscale.com/net/dnscache"
 	"tailscale.com/net/netknob"
 	"tailscale.com/net/netmon"
@@ -66,6 +68,8 @@ type Dialer struct {
 	netnsDialerOnce sync.Once
 	netnsDialer     netns.Dialer
 
+	routes atomic.Pointer[bart.Table[bool]] // or nil if UserDial should not use routes. `true` indicates routes that point into the Tailscale interface
+
 	mu               sync.Mutex
 	closed           bool
 	dns              dnsMap
@@ -129,6 +133,23 @@ func (d *Dialer) SetExitDNSDoH(doh string) {
 	}
 }
 
+// SetRoutes configures the dialer to dial the specified routes via Tailscale,
+// and the specified localRoutes using the default interface.
+func (d *Dialer) SetRoutes(routes, localRoutes []netip.Prefix) {
+	var rt *bart.Table[bool]
+	if len(routes) > 0 || len(localRoutes) > 0 {
+		rt = &bart.Table[bool]{}
+		for _, r := range routes {
+			rt.Insert(r, true)
+		}
+		for _, r := range localRoutes {
+			rt.Insert(r, false)
+		}
+	}
+
+	d.routes.Store(rt)
+}
+
 func (d *Dialer) Close() error {
 	d.mu.Lock()
 	defer d.mu.Unlock()
@@ -387,6 +408,15 @@ func (d *Dialer) UserDial(ctx context.Context, network, addr string) (net.Conn,
 		}
 		return d.NetstackDialTCP(ctx, ipp)
 	}
+
+	if routes := d.routes.Load(); routes != nil {
+		if isTailscaleRoute, _ := routes.Get(ipp.Addr()); isTailscaleRoute {
+			return d.getPeerDialer().DialContext(ctx, network, ipp.String())
+		}
+
+		return d.SystemDial(ctx, network, ipp.String())
+	}
+
 	// Workaround for macOS for now: dial Tailscale IPs with peer dialer.
 	// TODO(bradfitz): fix dialing subnet routers, public IPs via exit nodes,
 	// etc. This is a temporary partial for macOS. We need to plumb ART tables &
@@ -424,7 +454,7 @@ func (d *Dialer) dialPeerAPI(ctx context.Context, network, addr string) (net.Con
 }
 
 // getPeerDialer returns the *net.Dialer to use to dial peers (e.g. for peerapi,
-// or "tailscale nc")
+// "tailscale nc", or querying internal DNS servers over Tailscale)
 //
 // This is not used in netstack mode.
 //
diff --git a/tailcfg/tailcfg.go b/tailcfg/tailcfg.go
index dbe9daa8b..11f67386d 100644
--- a/tailcfg/tailcfg.go
+++ b/tailcfg/tailcfg.go
@@ -132,7 +132,8 @@
 //   - 89: 2024-03-23: Client no longer respects deleted PeerChange.Capabilities (use CapMap)
 //   - 90: 2024-04-03: Client understands PeerCapabilityTaildrive.
 //   - 91: 2024-04-24: Client understands PeerCapabilityTaildriveSharer.
-const CurrentCapabilityVersion CapabilityVersion = 91
+//   - 92: 2024-05-06: Client understands NodeAttrUserDialUseRoutes.
+const CurrentCapabilityVersion CapabilityVersion = 92
 
 type StableID string
 
@@ -2259,6 +2260,10 @@ type Oauth2Token struct {
 
 	// NodeAttrSuggestExitNodeUI allows the currently suggested exit node to appear in the client GUI.
 	NodeAttrSuggestExitNodeUI NodeCapability = "suggest-exit-node-ui"
+
+	// NodeAttrUserDialUseRoutes makes UserDial use either the peer dialer or the system dialer,
+	// depending on the destination address and the configured routes.
+	NodeAttrUserDialUseRoutes NodeCapability = "user-dial-routes"
 )
 
 // SetDNSRequest is a request to add a DNS record.