diff --git a/tlsutil/config.go b/tlsutil/config.go
index 7d658efea..0fad12716 100644
--- a/tlsutil/config.go
+++ b/tlsutil/config.go
@@ -326,7 +326,7 @@ func (c *Configurator) check(config Config, pool *x509.CertPool, cert *tls.Certi
 		if pool == nil {
 			return fmt.Errorf("VerifyIncoming set, and no CA certificate provided!")
 		}
-		if cert == nil || cert.Certificate == nil {
+		if cert == nil {
 			return fmt.Errorf("VerifyIncoming set, and no Cert/Key pair provided!")
 		}
 	}
@@ -351,7 +351,7 @@ func (c *Config) baseVerifyIncoming() bool {
 
 func loadKeyPair(certFile, keyFile string) (*tls.Certificate, error) {
 	if certFile == "" || keyFile == "" {
-		return &tls.Certificate{}, nil
+		return nil, nil
 	}
 	cert, err := tls.LoadX509KeyPair(certFile, keyFile)
 	if err != nil {
@@ -428,11 +428,16 @@ func (c *Configurator) commonTLSConfig(verifyIncoming bool) *tls.Config {
 	tlsConfig.PreferServerCipherSuites = c.base.PreferServerCipherSuites
 
 	// GetCertificate is used when acting as a server and responding to
-	// client requests. Always return the manually configured cert, because
-	// on the server this is all we have. And on the client, this is the
-	// only sensitive option.
+	// client requests. Default to the manually configured cert, but allow
+	// autoEncrypt cert too so that a client can encrypt incoming
+	// connections without having a manual cert configured.
 	tlsConfig.GetCertificate = func(*tls.ClientHelloInfo) (*tls.Certificate, error) {
-		return c.manual.cert, nil
+		cert := c.manual.cert
+		if cert == nil {
+			cert = c.autoEncrypt.cert
+		}
+
+		return cert, nil
 	}
 
 	// GetClientCertificate is used when acting as a client and responding
@@ -630,9 +635,9 @@ func (c *Configurator) OutgoingRPCWrapper() DCWrapper {
 // there is no cert, it will return a time in the past.
 func (c *Configurator) AutoEncryptCertNotAfter() time.Time {
 	c.RLock()
+	defer c.RUnlock()
 	tlsCert := c.autoEncrypt.cert
-	c.RUnlock()
-	if tlsCert == nil {
+	if tlsCert == nil || tlsCert.Certificate == nil {
 		return time.Now().AddDate(0, 0, -1)
 	}
 	cert, err := x509.ParseCertificate(tlsCert.Certificate[0])
diff --git a/tlsutil/config_test.go b/tlsutil/config_test.go
index 049130236..21d4a5740 100644
--- a/tlsutil/config_test.go
+++ b/tlsutil/config_test.go
@@ -293,17 +293,16 @@ func TestConfigurator_loadKeyPair(t *testing.T) {
 		cert, key string
 		shoulderr bool
 		isnil     bool
-		isempty   bool
 	}
 	variants := []variant{
-		{"", "", false, false, true},
-		{"bogus", "", false, false, true},
-		{"", "bogus", false, false, true},
-		{"../test/key/ourdomain.cer", "", false, false, true},
-		{"", "../test/key/ourdomain.key", false, false, true},
-		{"bogus", "bogus", true, true, false},
+		{"", "", false, true},
+		{"bogus", "", false, true},
+		{"", "bogus", false, true},
+		{"../test/key/ourdomain.cer", "", false, true},
+		{"", "../test/key/ourdomain.key", false, true},
+		{"bogus", "bogus", true, true},
 		{"../test/key/ourdomain.cer", "../test/key/ourdomain.key",
-			false, false, false},
+			false, false},
 	}
 	for i, v := range variants {
 		info := fmt.Sprintf("case %d", i)
@@ -317,10 +316,6 @@ func TestConfigurator_loadKeyPair(t *testing.T) {
 			require.NoError(t, err1, info)
 			require.NoError(t, err2, info)
 		}
-		if v.isempty {
-			require.Empty(t, cert1.Certificate, info)
-			require.Empty(t, cert2.Certificate, info)
-		}
 		if v.isnil {
 			require.Nil(t, cert1, info)
 			require.Nil(t, cert2, info)
@@ -538,17 +533,47 @@ func TestConfigurator_CommonTLSConfigGetClientCertificate(t *testing.T) {
 	c, err := NewConfigurator(Config{}, nil)
 	require.NoError(t, err)
 
-	cert, err := c.commonTLSConfig(false).GetCertificate(nil)
+	cert, err := c.commonTLSConfig(false).GetClientCertificate(nil)
 	require.NoError(t, err)
-	require.Nil(t, cert.Certificate)
+	require.Nil(t, cert)
 
-	c.manual.cert = &tls.Certificate{}
-	cert, err = c.commonTLSConfig(false).GetCertificate(nil)
+	c1, err := loadKeyPair("../test/key/something_expired.cer", "../test/key/something_expired.key")
+	require.NoError(t, err)
+	c.manual.cert = c1
+	cert, err = c.commonTLSConfig(false).GetClientCertificate(nil)
 	require.NoError(t, err)
 	require.Equal(t, c.manual.cert, cert)
 
+	c2, err := loadKeyPair("../test/key/ourdomain.cer", "../test/key/ourdomain.key")
+	require.NoError(t, err)
+	c.autoEncrypt.cert = c2
 	cert, err = c.commonTLSConfig(false).GetClientCertificate(nil)
 	require.NoError(t, err)
+	require.Equal(t, c.autoEncrypt.cert, cert)
+}
+
+func TestConfigurator_CommonTLSConfigGetCertificate(t *testing.T) {
+	c, err := NewConfigurator(Config{}, nil)
+	require.NoError(t, err)
+
+	cert, err := c.commonTLSConfig(false).GetCertificate(nil)
+	require.NoError(t, err)
+	require.Nil(t, cert)
+
+	// Setting a certificate as the auto-encrypt cert will return it as the regular server certificate
+	c1, err := loadKeyPair("../test/key/something_expired.cer", "../test/key/something_expired.key")
+	require.NoError(t, err)
+	c.autoEncrypt.cert = c1
+	cert, err = c.commonTLSConfig(false).GetCertificate(nil)
+	require.NoError(t, err)
+	require.Equal(t, c.autoEncrypt.cert, cert)
+
+	// Setting a different certificate as a manual cert will override the auto-encrypt cert and instead return the manual cert
+	c2, err := loadKeyPair("../test/key/ourdomain.cer", "../test/key/ourdomain.key")
+	require.NoError(t, err)
+	c.manual.cert = c2
+	cert, err = c.commonTLSConfig(false).GetCertificate(nil)
+	require.NoError(t, err)
 	require.Equal(t, c.manual.cert, cert)
 }
 
@@ -715,7 +740,7 @@ func TestConfigurator_UpdateSetsStuff(t *testing.T) {
 	c, err := NewConfigurator(Config{}, nil)
 	require.NoError(t, err)
 	require.Nil(t, c.caPool)
-	require.Nil(t, c.manual.cert.Certificate)
+	require.Nil(t, c.manual.cert)
 	require.Equal(t, c.base, &Config{})
 	require.Equal(t, 1, c.version)