diff --git a/cmd/contour/servecontext.go b/cmd/contour/servecontext.go
index f2a662fa0cc..151467349f6 100644
--- a/cmd/contour/servecontext.go
+++ b/cmd/contour/servecontext.go
@@ -221,6 +221,7 @@ func (ctx *serveContext) tlsconfig() *tls.Config {
 	err := ctx.verifyTLSFlags()
 	check(err)
 
+	// load certificates and key to catch configuration errors early
 	cert, err := tls.LoadX509KeyPair(ctx.contourCert, ctx.contourKey)
 	check(err)
 
@@ -232,11 +233,33 @@ func (ctx *serveContext) tlsconfig() *tls.Config {
 		log.Fatalf("unable to append certificate in %s to CA pool", ctx.caFile)
 	}
 
+	// lazily load certificates and key at TLS handshake to ensure that latest
+	// certificates are used in case they have been rotated
 	return &tls.Config{
 		Certificates: []tls.Certificate{cert},
 		ClientAuth:   tls.RequireAndVerifyClientCert,
 		ClientCAs:    certPool,
 		Rand:         rand.Reader,
+		GetConfigForClient: func(*tls.ClientHelloInfo) (*tls.Config, error) {
+
+			cert, err := tls.LoadX509KeyPair(ctx.contourCert, ctx.contourKey)
+			check(err)
+
+			ca, err := ioutil.ReadFile(ctx.caFile)
+			check(err)
+
+			certPool := x509.NewCertPool()
+			if ok := certPool.AppendCertsFromPEM(ca); !ok {
+				log.Fatalf("unable to append certificate in %s to CA pool", ctx.caFile)
+			}
+
+			return &tls.Config{
+				Certificates: []tls.Certificate{cert},
+				ClientAuth:   tls.RequireAndVerifyClientCert,
+				ClientCAs:    certPool,
+				Rand:         rand.Reader,
+			}, nil
+		},
 	}
 }
 
diff --git a/cmd/contour/servecontext_test.go b/cmd/contour/servecontext_test.go
index db5ccc3b6c7..7de16cec88c 100644
--- a/cmd/contour/servecontext_test.go
+++ b/cmd/contour/servecontext_test.go
@@ -14,11 +14,20 @@
 package main
 
 import (
+	"crypto/tls"
+	"crypto/x509"
+	"encoding/pem"
+	"io/ioutil"
+	"net"
+	"os"
+	"path/filepath"
 	"reflect"
 	"testing"
 	"time"
 
 	"github.com/google/go-cmp/cmp"
+	"github.com/projectcontour/contour/internal/assert"
+	"google.golang.org/grpc"
 	"gopkg.in/yaml.v2"
 )
 
@@ -191,9 +200,167 @@ leaderelection:
 	}
 }
 
+// testdata for this test case can be re-generated by running:
+// make gencerts
+// cp certs/*.pem cmd/contour/testdata/X/
+func TestServeContextCertificateHandling(t *testing.T) {
+	tests := map[string]struct {
+		serverCredentialsDir string
+		clientCredentialsDir string
+		expectedServerCert   string
+		expectError          bool
+	}{
+		"successful TLS connection established": {
+			serverCredentialsDir: "testdata/1",
+			clientCredentialsDir: "testdata/1",
+			expectedServerCert:   "testdata/1/contourcert.pem",
+			expectError:          false,
+		},
+		"rotating server credentials returns new server cert": {
+			serverCredentialsDir: "testdata/2",
+			clientCredentialsDir: "testdata/2",
+			expectedServerCert:   "testdata/2/contourcert.pem",
+			expectError:          false,
+		},
+		"fail to connect with bad client certificate": {
+			serverCredentialsDir: "testdata/2",
+			clientCredentialsDir: "testdata/1",
+			expectedServerCert:   "testdata/2/contourcert.pem",
+			expectError:          true,
+		},
+	}
+
+	// create temporary directory to store certificates and key for the server
+	configDir, err := ioutil.TempDir("", "contour-testdata-")
+	checkErr(t, err)
+	defer os.RemoveAll(configDir)
+
+	ctx := serveContext{
+		caFile:      filepath.Join(configDir, "CAcert.pem"),
+		contourCert: filepath.Join(configDir, "contourcert.pem"),
+		contourKey:  filepath.Join(configDir, "contourkey.pem"),
+	}
+
+	// initial set of credentials must be linked into temp directory before
+	// starting the tests, to avoid error at server startup
+	err = linkFiles("testdata/1", configDir)
+	checkErr(t, err)
+
+	// start a dummy server
+	opts := ctx.grpcOptions()
+	g := grpc.NewServer(opts...)
+	if g == nil {
+		t.Error("failed to create server")
+	}
+
+	address := "localhost:8001"
+	l, err := net.Listen("tcp", address)
+	checkErr(t, err)
+
+	go func() {
+		err = g.Serve(l)
+		checkErr(t, err)
+	}()
+	defer g.Stop()
+
+	for name, tc := range tests {
+		t.Run(name, func(t *testing.T) {
+			// link certificates and key to temp dir used by serveContext
+			err = linkFiles(tc.serverCredentialsDir, configDir)
+			checkErr(t, err)
+			receivedCert, err := tryConnect(address, tc.clientCredentialsDir)
+			gotError := err != nil
+			if gotError != tc.expectError {
+				t.Errorf("Unexpected result when connecting to the server: %s", err)
+			}
+			if err == nil {
+				expectedCert, err := loadCertificate(tc.expectedServerCert)
+				checkErr(t, err)
+				assert.Equal(t, receivedCert, expectedCert)
+			}
+		})
+	}
+}
+
 func checkErr(t *testing.T, err error) {
 	t.Helper()
 	if err != nil {
 		t.Error(err)
 	}
 }
+
+// create symbolic link of files in src directory to the dst directory
+func linkFiles(src string, dst string) error {
+	absSrc, err := filepath.Abs(src)
+	if err != nil {
+		return err
+	}
+
+	matches, err := filepath.Glob(filepath.Join(absSrc, "*"))
+	if err != nil {
+		return err
+	}
+
+	for _, filename := range matches {
+		basename := filepath.Base(filename)
+		os.Remove(filepath.Join(dst, basename))
+		err := os.Symlink(filename, filepath.Join(dst, basename))
+		if err != nil {
+			return err
+		}
+	}
+
+	return nil
+}
+
+// try to establish TLS connection to the server, if successful, return the server certificate
+func tryConnect(address string, clientCredentialsDir string) (*x509.Certificate, error) {
+	clientCert := filepath.Join(clientCredentialsDir, "envoycert.pem")
+	clientKey := filepath.Join(clientCredentialsDir, "envoykey.pem")
+	cert, err := tls.LoadX509KeyPair(clientCert, clientKey)
+	if err != nil {
+		return nil, err
+	}
+
+	clientConfig := &tls.Config{
+		ServerName:         "localhost",
+		Certificates:       []tls.Certificate{cert},
+		InsecureSkipVerify: true,
+	}
+	conn, err := tls.Dial("tcp", address, clientConfig)
+	if err != nil {
+		return nil, err
+	}
+	defer conn.Close()
+
+	err = peekError(conn)
+	if err != nil {
+		return nil, err
+	}
+
+	return conn.ConnectionState().PeerCertificates[0], nil
+}
+
+func loadCertificate(path string) (*x509.Certificate, error) {
+	buf, err := ioutil.ReadFile(path)
+	if err != nil {
+		return nil, err
+	}
+	block, _ := pem.Decode(buf)
+	return x509.ParseCertificate(block.Bytes)
+}
+
+// Workaround for TLS 1.3: due to shortened handshake, TLS alert from server is
+// received at first read from the socket. To receive alert for bad certificate,
+// this function tries to read one byte.
+// Adapted from https://golang.org/src/crypto/tls/handshake_client_test.go
+func peekError(conn net.Conn) error {
+	_ = conn.SetReadDeadline(time.Now().Add(100 * time.Millisecond))
+	_, err := conn.Read(make([]byte, 1))
+	if err != nil {
+		if netErr, ok := err.(net.Error); !ok || !netErr.Timeout() {
+			return err
+		}
+	}
+	return nil
+}
diff --git a/cmd/contour/testdata/1/CAcert.pem b/cmd/contour/testdata/1/CAcert.pem
new file mode 100644
index 00000000000..e80dc9ac283
--- /dev/null
+++ b/cmd/contour/testdata/1/CAcert.pem
@@ -0,0 +1,20 @@
+-----BEGIN CERTIFICATE-----
+MIIDPzCCAiegAwIBAgIUHA9n4BBwtiDHvIN4Eq8isFCk+3wwDQYJKoZIhvcNAQEL
+BQAwLzEYMBYGA1UECgwPUHJvamVjdCBDb250b3VyMRMwEQYDVQQDDApDb250b3Vy
+IENBMB4XDTIwMDEyOTE1MzkyNFoXDTI1MDEyNzE1MzkyNFowLzEYMBYGA1UECgwP
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+0BKyceVWKfbvn23kc47xylFkFQnmbYxIEkJA4/Jq6ewsBScB1mp24s+xyl1m6ePO
+WhMo7Od2xQsUhGKDJYMFV7cXmwDXR2QudZE+OvcaSoVYMktOpyh07RSRQEkx4URY
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+87uOS8Z1n+Sxw5fKH1rp/TVbwm++nVJ7RjalRQBG5skdx6J7qEL9H2vx9VHG/7Ib
+G+NL95TBtk9042KJFiZXsY8KPA4JSEFPWVIcXmaq2iTJxSMHGD3MQv33yjgXH81U
+e09f27Vfbl+YFvkSljZJKxXjgwPVDlo5Sv/9e4mS51dhraEvJV+dubz7EVv/R7F/
+pHX+tVn0+WSfero8cIfhhj1H9+Cn5lnUUHYnnnbrLh5j8ZldniW2nXkOWR5LQN0J
+CwkA744hrtGj9dDmI/vwcpQ1tw==
+-----END CERTIFICATE-----
diff --git a/cmd/contour/testdata/1/CAkey.pem b/cmd/contour/testdata/1/CAkey.pem
new file mode 100644
index 00000000000..0a5872db217
--- /dev/null
+++ b/cmd/contour/testdata/1/CAkey.pem
@@ -0,0 +1,28 @@
+-----BEGIN PRIVATE KEY-----
+MIIEvgIBADANBgkqhkiG9w0BAQEFAASCBKgwggSkAgEAAoIBAQDJf6bt4nNgscFE
+hoN+2AOi8GO0wZAnyPM17MVzq4To9yxCGTuciPwLOB3wmv8CwdjxrjH8912bzp1j
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+HTS5+5+m8y3RxoThspWO8DkY
+-----END PRIVATE KEY-----
diff --git a/cmd/contour/testdata/1/contourcert.pem b/cmd/contour/testdata/1/contourcert.pem
new file mode 100644
index 00000000000..d92d8a801ea
--- /dev/null
+++ b/cmd/contour/testdata/1/contourcert.pem
@@ -0,0 +1,21 @@
+-----BEGIN CERTIFICATE-----
+MIIDhzCCAm+gAwIBAgIUQ791kdZBTnbqToyBUaKKLuIaqqYwDQYJKoZIhvcNAQEL
+BQAwLzEYMBYGA1UECgwPUHJvamVjdCBDb250b3VyMRMwEQYDVQQDDApDb250b3Vy
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+hZyX+069Mi553cRwd95hWPzttJVSrNhvRCj91IpZgTYEUHLWvWhhs36xFg==
+-----END CERTIFICATE-----
diff --git a/cmd/contour/testdata/1/contourkey.pem b/cmd/contour/testdata/1/contourkey.pem
new file mode 100644
index 00000000000..e6e093be313
--- /dev/null
+++ b/cmd/contour/testdata/1/contourkey.pem
@@ -0,0 +1,27 @@
+-----BEGIN RSA PRIVATE KEY-----
+MIIEowIBAAKCAQEAw6pOu3k8fO6TejESmIKuTFGIuZf/PW86cMImfeHwDahGVffv
+bLTK0YNpTeeyuACFH3vgMPMhBpPUVRK/te8cK02kWQGNROQgQMM9KKyby//zQTze
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+WwSKVFuctBnrT2ZDTtfhAtIQ8ebkF2kUOhmLmwfaRismiIPt4Nwu
+-----END RSA PRIVATE KEY-----
diff --git a/cmd/contour/testdata/1/envoycert.pem b/cmd/contour/testdata/1/envoycert.pem
new file mode 100644
index 00000000000..1ab7aad52b1
--- /dev/null
+++ b/cmd/contour/testdata/1/envoycert.pem
@@ -0,0 +1,20 @@
+-----BEGIN CERTIFICATE-----
+MIIDPzCCAiegAwIBAgIUQ791kdZBTnbqToyBUaKKLuIaqqcwDQYJKoZIhvcNAQEL
+BQAwLzEYMBYGA1UECgwPUHJvamVjdCBDb250b3VyMRMwEQYDVQQDDApDb250b3Vy
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+cUa45Lfpy5XmCzB+wAISoGvqlQ==
+-----END CERTIFICATE-----
diff --git a/cmd/contour/testdata/1/envoykey.pem b/cmd/contour/testdata/1/envoykey.pem
new file mode 100644
index 00000000000..6bd76042ee3
--- /dev/null
+++ b/cmd/contour/testdata/1/envoykey.pem
@@ -0,0 +1,27 @@
+-----BEGIN RSA PRIVATE KEY-----
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+2U4s19wtV9g3rDVbPgpGQZSl0uvF+uVMijfF5mlMy4aQQYCG1eUKpbc=
+-----END RSA PRIVATE KEY-----
diff --git a/cmd/contour/testdata/2/CAcert.pem b/cmd/contour/testdata/2/CAcert.pem
new file mode 100644
index 00000000000..285c1b7c191
--- /dev/null
+++ b/cmd/contour/testdata/2/CAcert.pem
@@ -0,0 +1,20 @@
+-----BEGIN CERTIFICATE-----
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+/8R1NmX7im8Rxbbi7neK2V/QSQ==
+-----END CERTIFICATE-----
diff --git a/cmd/contour/testdata/2/CAkey.pem b/cmd/contour/testdata/2/CAkey.pem
new file mode 100644
index 00000000000..e2b151de00d
--- /dev/null
+++ b/cmd/contour/testdata/2/CAkey.pem
@@ -0,0 +1,28 @@
+-----BEGIN PRIVATE KEY-----
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+D6U0mFbSCrcw/a2axq9jYQpp
+-----END PRIVATE KEY-----
diff --git a/cmd/contour/testdata/2/contourcert.pem b/cmd/contour/testdata/2/contourcert.pem
new file mode 100644
index 00000000000..5479c74b4d8
--- /dev/null
+++ b/cmd/contour/testdata/2/contourcert.pem
@@ -0,0 +1,21 @@
+-----BEGIN CERTIFICATE-----
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+-----END CERTIFICATE-----
diff --git a/cmd/contour/testdata/2/contourkey.pem b/cmd/contour/testdata/2/contourkey.pem
new file mode 100644
index 00000000000..5d471ac1652
--- /dev/null
+++ b/cmd/contour/testdata/2/contourkey.pem
@@ -0,0 +1,27 @@
+-----BEGIN RSA PRIVATE KEY-----
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+ubVZrIIz3O+RkhFZUhHCKXUCkp8ZDTKKgffC18yO1i+u2QBDmg8=
+-----END RSA PRIVATE KEY-----
diff --git a/cmd/contour/testdata/2/envoycert.pem b/cmd/contour/testdata/2/envoycert.pem
new file mode 100644
index 00000000000..8c073e529f6
--- /dev/null
+++ b/cmd/contour/testdata/2/envoycert.pem
@@ -0,0 +1,20 @@
+-----BEGIN CERTIFICATE-----
+MIIDPzCCAiegAwIBAgIUU2yskngkWNirZxeWaCsOv457Ok8wDQYJKoZIhvcNAQEL
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+sfMITrj/e/7I3FjxL82OPLBcJg==
+-----END CERTIFICATE-----
diff --git a/cmd/contour/testdata/2/envoykey.pem b/cmd/contour/testdata/2/envoykey.pem
new file mode 100644
index 00000000000..6361ff0d277
--- /dev/null
+++ b/cmd/contour/testdata/2/envoykey.pem
@@ -0,0 +1,27 @@
+-----BEGIN RSA PRIVATE KEY-----
+MIIEogIBAAKCAQEAxVLXVI8t9WWXqOlRBJT1zLAfdbvfLcCAUFuHRKO1oVQE+1md
+InJQji2oSa0Io6PpeLFubFrS3kislMzG5PF4mCvKdmlgYwzRu4Dx9COr4wGPPSND
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+-----END RSA PRIVATE KEY-----