diff --git a/net/dns/manager_openbsd.go b/net/dns/manager_openbsd.go
index 2889bbf0b..e1611d3cc 100644
--- a/net/dns/manager_openbsd.go
+++ b/net/dns/manager_openbsd.go
@@ -4,8 +4,71 @@
 
 package dns
 
-import "tailscale.com/types/logger"
+import (
+	"bytes"
+	"fmt"
+	"os"
 
-func NewOSConfigurator(logf logger.Logf, _ string) (OSConfigurator, error) {
+	"tailscale.com/types/logger"
+)
+
+type kv struct {
+	k, v string
+}
+
+func (kv kv) String() string {
+	return fmt.Sprintf("%s=%s", kv.k, kv.v)
+}
+
+func NewOSConfigurator(logf logger.Logf, interfaceName string) (OSConfigurator, error) {
+	return newOSConfigurator(logf, interfaceName,
+		newOSConfigEnv{
+			rcIsResolvd: rcIsResolvd,
+			fs:          directFS{},
+		})
+}
+
+// newOSConfigEnv are the funcs newOSConfigurator needs, pulled out for testing.
+type newOSConfigEnv struct {
+	fs          directFS
+	rcIsResolvd func(resolvConfContents []byte) bool
+}
+
+func newOSConfigurator(logf logger.Logf, interfaceName string, env newOSConfigEnv) (ret OSConfigurator, err error) {
+	var debug []kv
+	dbg := func(k, v string) {
+		debug = append(debug, kv{k, v})
+	}
+	defer func() {
+		if ret != nil {
+			dbg("ret", fmt.Sprintf("%T", ret))
+		}
+		logf("dns: %v", debug)
+	}()
+
+	bs, err := env.fs.ReadFile(resolvConf)
+	if os.IsNotExist(err) {
+		dbg("rc", "missing")
+		return newDirectManager(logf), nil
+	}
+	if err != nil {
+		return nil, fmt.Errorf("reading /etc/resolv.conf: %w", err)
+	}
+
+	if env.rcIsResolvd(bs) {
+		dbg("resolvd", "yes")
+		return newResolvdManager(logf, interfaceName)
+	}
+
+	dbg("resolvd", "missing")
 	return newDirectManager(logf), nil
 }
+
+func rcIsResolvd(resolvConfContents []byte) bool {
+	// If we have the string "# resolvd:" in resolv.conf resolvd(8) is
+	// managing things.
+	if bytes.Contains(resolvConfContents, []byte("# resolvd:")) {
+		return true
+	}
+	return false
+}
diff --git a/net/dns/resolvd.go b/net/dns/resolvd.go
new file mode 100644
index 000000000..42b09ee5a
--- /dev/null
+++ b/net/dns/resolvd.go
@@ -0,0 +1,141 @@
+// Copyright (c) 2020 Tailscale Inc & AUTHORS All rights reserved.
+// Use of this source code is governed by a BSD-style
+// license that can be found in the LICENSE file.
+
+//go:build openbsd
+// +build openbsd
+
+package dns
+
+import (
+	"bufio"
+	"bytes"
+	"fmt"
+	"os"
+	"os/exec"
+	"regexp"
+	"strings"
+
+	"tailscale.com/types/logger"
+	"tailscale.com/util/dnsname"
+)
+
+func newResolvdManager(logf logger.Logf, interfaceName string) (*resolvdManager, error) {
+	return &resolvdManager{
+		logf:   logf,
+		ifName: interfaceName,
+		fs:     directFS{},
+	}, nil
+}
+
+// resolvdManager is an OSConfigurator which uses route(1) to teach OpenBSD's
+// resolvd(8) about DNS servers.
+type resolvdManager struct {
+	logf   logger.Logf
+	ifName string
+	fs     directFS
+}
+
+func (m *resolvdManager) SetDNS(config OSConfig) error {
+	args := []string{
+		"nameserver",
+		m.ifName,
+	}
+
+	origResolv, err := m.readAndCopy(resolvConf, backupConf, 0644)
+	if err != nil {
+		return err
+	}
+	newResolvConf := removeSearchLines(origResolv)
+
+	for _, ns := range config.Nameservers {
+		args = append(args, ns.String())
+	}
+
+	var newSearch = []string{
+		"search",
+	}
+	for _, s := range config.SearchDomains {
+		newSearch = append(newSearch, s.WithoutTrailingDot())
+	}
+
+	newResolvConf = append(newResolvConf, []byte(strings.Join(newSearch, " "))...)
+
+	err = m.fs.WriteFile(resolvConf, newResolvConf, 0644)
+	if err != nil {
+		return err
+	}
+
+	cmd := exec.Command("/sbin/route", args...)
+	return cmd.Run()
+}
+
+func (m *resolvdManager) SupportsSplitDNS() bool {
+	return false
+}
+
+func (m *resolvdManager) GetBaseConfig() (OSConfig, error) {
+	cfg, err := m.readResolvConf()
+	if err != nil {
+		return OSConfig{}, err
+	}
+
+	return cfg, nil
+}
+
+func (m *resolvdManager) Close() error {
+	// resolvd handles teardown of nameservers so we only need to write back the original
+	// config and be done.
+
+	_, err := m.readAndCopy(backupConf, resolvConf, 0644)
+	if err != nil {
+		return err
+	}
+
+	return m.fs.Remove(backupConf)
+}
+
+func (m *resolvdManager) readAndCopy(a, b string, mode os.FileMode) ([]byte, error) {
+	orig, err := m.fs.ReadFile(a)
+	if err != nil {
+		return nil, err
+	}
+	err = m.fs.WriteFile(b, orig, mode)
+	if err != nil {
+		return nil, err
+	}
+
+	return orig, nil
+}
+
+func (m resolvdManager) readResolvConf() (config OSConfig, err error) {
+	b, err := m.fs.ReadFile(resolvConf)
+	if err != nil {
+		return OSConfig{}, err
+	}
+
+	scanner := bufio.NewScanner(bytes.NewReader(b))
+	for scanner.Scan() {
+		line := strings.TrimSpace(scanner.Text())
+
+		// resolvd manages "nameserver" lines, we only need to handle
+		// "search".
+		if strings.HasPrefix(line, "search") {
+			domain := strings.TrimPrefix(line, "search")
+			domain = strings.TrimSpace(domain)
+			fqdn, err := dnsname.ToFQDN(domain)
+			if err != nil {
+				return OSConfig{}, fmt.Errorf("parsing search domains %q: %w", line, err)
+			}
+			config.SearchDomains = append(config.SearchDomains, fqdn)
+			continue
+		}
+	}
+
+	return config, nil
+}
+
+func removeSearchLines(orig []byte) []byte {
+	re := regexp.MustCompile(`(?m)^search\s+.+$`)
+	return re.ReplaceAll(orig, []byte(""))
+}