diff --git a/net/dns/direct.go b/net/dns/direct.go
index ec2e42e75..f6f2fd601 100644
--- a/net/dns/direct.go
+++ b/net/dns/direct.go
@@ -442,7 +442,9 @@ func (m *directManager) runFileWatcher() {
 	if !ok {
 		return
 	}
-	if err := watchFile(m.ctx, "/etc/", resolvConf, m.checkForFileTrample); err != nil {
+	dir := m.fs.ActualPath(filepath.Dir(resolvConf))
+	file := m.fs.ActualPath(resolvConf)
+	if err := watchFile(m.ctx, dir, file, m.checkForFileTrample); err != nil {
 		// This is all best effort for now, so surface warnings to users.
 		m.logf("dns: inotify: %s", err)
 	}
@@ -597,6 +599,19 @@ type wholeFileFS interface {
 	ReadFile(name string) ([]byte, error)
 	Remove(name string) error
 	Rename(oldName, newName string) error
+	// ActualPath returns the real filesystem path for the given absolute
+	// logical path. All other methods in this interface accept logical
+	// paths (like "/etc/resolv.conf") and translate them internally;
+	// ActualPath exposes that same translation for callers that need
+	// the real path for use outside the interface (e.g. setting up an
+	// inotify watch on the correct directory).
+	//
+	// For directFS with an empty prefix (production), the input is
+	// returned unchanged ("/etc" → "/etc"). For directFS with a test
+	// prefix like "/tmp/test123", the prefix is joined
+	// ("/etc" → "/tmp/test123/etc"). For wslFS the input is returned
+	// unchanged, since paths are passed through to wsl.exe as-is.
+	ActualPath(name string) string
 	Stat(name string) (isRegular bool, err error)
 	Truncate(name string) error
 	WriteFile(name string, contents []byte, perm os.FileMode) error
@@ -613,6 +628,8 @@ type directFS struct {
 
 func (fs directFS) path(name string) string { return filepath.Join(fs.prefix, name) }
 
+func (fs directFS) ActualPath(name string) string { return fs.path(name) }
+
 func (fs directFS) Stat(name string) (isRegular bool, err error) {
 	fi, err := os.Stat(fs.path(name))
 	if err != nil {
diff --git a/net/dns/direct_linux_test.go b/net/dns/direct_linux_test.go
index 9955a863f..c053db178 100644
--- a/net/dns/direct_linux_test.go
+++ b/net/dns/direct_linux_test.go
@@ -7,14 +7,12 @@ package dns
 
 import (
 	"context"
-	"fmt"
 	"net/netip"
 	"os"
 	"path/filepath"
 	"testing"
 	"testing/synctest"
-
-	"github.com/illarion/gonotify/v3"
+	"time"
 
 	"tailscale.com/util/dnsname"
 	"tailscale.com/util/eventbus/eventbustest"
@@ -77,33 +75,20 @@ search ts.net ts-dns.test
 	})
 }
 
-// watchFile is generally copied from linuxtrample, but cancels the context
-// after the first call to cb() after the first trample to end the test.
+// watchFile is a test implementation of the file watcher that uses a timer
+// instead of inotify. Real inotify (gonotify.NewDirWatcher) creates goroutines
+// that block on real syscalls, which don't work inside synctest's fake-time
+// bubble. Instead, we use a one-shot timer that synctest.Wait() will advance,
+// triggering a callback to check for file trampling.
 func watchFile(ctx context.Context, dir, filename string, cb func()) error {
-	ctx, cancel := context.WithCancel(ctx)
-	defer cancel()
-
-	const events = gonotify.IN_ATTRIB |
-		gonotify.IN_CLOSE_WRITE |
-		gonotify.IN_CREATE |
-		gonotify.IN_DELETE |
-		gonotify.IN_MODIFY |
-		gonotify.IN_MOVE
-
-	watcher, err := gonotify.NewDirWatcher(ctx, events, dir)
-	if err != nil {
-		return fmt.Errorf("NewDirWatcher: %w", err)
-	}
-
-	for {
-		select {
-		case event := <-watcher.C:
-			if event.Name == filename {
-				cb()
-				cancel()
-			}
-		case <-ctx.Done():
-			return ctx.Err()
-		}
+	timer := time.NewTimer(time.Millisecond)
+	defer timer.Stop()
+	select {
+	case <-ctx.Done():
+		return ctx.Err()
+	case <-timer.C:
+		cb()
 	}
+	<-ctx.Done()
+	return ctx.Err()
 }
diff --git a/net/dns/manager_linux_test.go b/net/dns/manager_linux_test.go
index a108a3297..c3c99307a 100644
--- a/net/dns/manager_linux_test.go
+++ b/net/dns/manager_linux_test.go
@@ -316,6 +316,7 @@ func (m memFS) Stat(name string) (isRegular bool, err error) {
 func (m memFS) Chmod(name string, mode os.FileMode) error { panic("TODO") }
 func (m memFS) Rename(oldName, newName string) error      { panic("TODO") }
 func (m memFS) Remove(name string) error                  { panic("TODO") }
+func (m memFS) ActualPath(name string) string             { return name }
 func (m memFS) ReadFile(name string) ([]byte, error) {
 	v, ok := m[name]
 	if !ok {
diff --git a/net/dns/wsl_windows.go b/net/dns/wsl_windows.go
index 1b93142f5..b0e62170b 100644
--- a/net/dns/wsl_windows.go
+++ b/net/dns/wsl_windows.go
@@ -148,6 +148,8 @@ type wslFS struct {
 	distro string
 }
 
+func (fs wslFS) ActualPath(name string) string { return name }
+
 func (fs wslFS) Stat(name string) (isRegular bool, err error) {
 	err = wslRun(fs.cmd("test", "-f", name))
 	if ee, _ := err.(*exec.ExitError); ee != nil {