diff --git a/pkg/daemons/control/deps/deps.go b/pkg/daemons/control/deps/deps.go
index be10d9ebca5f..6753e6c792ed 100644
--- a/pkg/daemons/control/deps/deps.go
+++ b/pkg/daemons/control/deps/deps.go
@@ -24,6 +24,7 @@ import (
 	"github.com/k3s-io/k3s/pkg/daemons/config"
 	"github.com/k3s-io/k3s/pkg/passwd"
 	"github.com/k3s-io/k3s/pkg/token"
+	"github.com/k3s-io/k3s/pkg/util"
 	"github.com/k3s-io/k3s/pkg/version"
 	certutil "github.com/rancher/dynamiclistener/cert"
 	"github.com/sirupsen/logrus"
@@ -592,7 +593,7 @@ func createClientCertKey(regen bool, commonName string, organization []string, a
 		return false, err
 	}
 
-	caCert, err := certutil.CertsFromFile(caCertFile)
+	caCerts, err := certutil.CertsFromFile(caCertFile)
 	if err != nil {
 		return false, err
 	}
@@ -615,12 +616,12 @@ func createClientCertKey(regen bool, commonName string, organization []string, a
 	if altNames != nil {
 		cfg.AltNames = *altNames
 	}
-	cert, err := certutil.NewSignedCert(cfg, key.(crypto.Signer), caCert[0], caKey.(crypto.Signer))
+	cert, err := certutil.NewSignedCert(cfg, key.(crypto.Signer), caCerts[0], caKey.(crypto.Signer))
 	if err != nil {
 		return false, err
 	}
 
-	return true, certutil.WriteCert(certFile, append(certutil.EncodeCertPEM(cert), certutil.EncodeCertPEM(caCert[0])...))
+	return true, certutil.WriteCert(certFile, util.EncodeCertsPEM(cert, caCerts))
 }
 
 func exists(files ...string) bool {
diff --git a/pkg/server/cert.go b/pkg/server/cert.go
index e90e2c6c4e35..db26f632cd7b 100644
--- a/pkg/server/cert.go
+++ b/pkg/server/cert.go
@@ -143,10 +143,6 @@ func validateCA(oldCAPath, newCAPath string) error {
 		return err
 	}
 
-	if len(oldCerts) == 1 {
-		return errors.New("old CA is self-signed")
-	}
-
 	newCerts, err := certutil.CertsFromFile(newCAPath)
 	if err != nil {
 		return err
@@ -158,16 +154,26 @@ func validateCA(oldCAPath, newCAPath string) error {
 
 	roots := x509.NewCertPool()
 	intermediates := x509.NewCertPool()
-	for i, cert := range oldCerts {
+
+	// Load all certs from the old bundle
+	for _, cert := range oldCerts {
+		if len(cert.AuthorityKeyId) == 0 || bytes.Equal(cert.AuthorityKeyId, cert.SubjectKeyId) {
+			roots.AddCert(cert)
+		} else {
+			intermediates.AddCert(cert)
+		}
+	}
+
+	// Include any intermediates from the new bundle, in case they're cross-signed by a cert in the old bundle
+	for i, cert := range newCerts {
 		if i > 0 {
-			if len(cert.AuthorityKeyId) == 0 || bytes.Equal(cert.AuthorityKeyId, cert.SubjectKeyId) {
-				roots.AddCert(cert)
-			} else {
+			if len(cert.AuthorityKeyId) > 0 {
 				intermediates.AddCert(cert)
 			}
 		}
 	}
 
+	// Verify the first cert in the bundle, using the combined roots and intermediates
 	_, err = newCerts[0].Verify(x509.VerifyOptions{Roots: roots, Intermediates: intermediates})
 	if err != nil {
 		err = errors.Wrap(err, "new CA cert cannot be verified using old CA chain")
diff --git a/pkg/server/router.go b/pkg/server/router.go
index 37169e1fe1b1..435e6b7fdf45 100644
--- a/pkg/server/router.go
+++ b/pkg/server/router.go
@@ -219,7 +219,7 @@ func servingKubeletCert(server *config.Control, keyFile string, auth nodePassBoo
 			return
 		}
 
-		caCert, caKey, key, err := getCACertAndKeys(server.Runtime.ServerCA, server.Runtime.ServerCAKey, server.Runtime.ServingKubeletKey)
+		caCerts, caKey, key, err := getCACertAndKeys(server.Runtime.ServerCA, server.Runtime.ServerCAKey, server.Runtime.ServingKubeletKey)
 		if err != nil {
 			sendError(err, resp)
 			return
@@ -245,7 +245,7 @@ func servingKubeletCert(server *config.Control, keyFile string, auth nodePassBoo
 				DNSNames: []string{nodeName, "localhost"},
 				IPs:      ips,
 			},
-		}, key, caCert[0], caKey)
+		}, key, caCerts[0], caKey)
 		if err != nil {
 			sendError(err, resp)
 			return
@@ -257,7 +257,7 @@ func servingKubeletCert(server *config.Control, keyFile string, auth nodePassBoo
 			return
 		}
 
-		resp.Write(append(certutil.EncodeCertPEM(cert), certutil.EncodeCertPEM(caCert[0])...))
+		resp.Write(util.EncodeCertsPEM(cert, caCerts))
 		resp.Write(keyBytes)
 	})
 }
@@ -275,7 +275,7 @@ func clientKubeletCert(server *config.Control, keyFile string, auth nodePassBoot
 			return
 		}
 
-		caCert, caKey, key, err := getCACertAndKeys(server.Runtime.ClientCA, server.Runtime.ClientCAKey, server.Runtime.ClientKubeletKey)
+		caCerts, caKey, key, err := getCACertAndKeys(server.Runtime.ClientCA, server.Runtime.ClientCAKey, server.Runtime.ClientKubeletKey)
 		if err != nil {
 			sendError(err, resp)
 			return
@@ -285,7 +285,7 @@ func clientKubeletCert(server *config.Control, keyFile string, auth nodePassBoot
 			CommonName:   "system:node:" + nodeName,
 			Organization: []string{user.NodesGroup},
 			Usages:       []x509.ExtKeyUsage{x509.ExtKeyUsageClientAuth},
-		}, key, caCert[0], caKey)
+		}, key, caCerts[0], caKey)
 		if err != nil {
 			sendError(err, resp)
 			return
@@ -297,7 +297,7 @@ func clientKubeletCert(server *config.Control, keyFile string, auth nodePassBoot
 			return
 		}
 
-		resp.Write(append(certutil.EncodeCertPEM(cert), certutil.EncodeCertPEM(caCert[0])...))
+		resp.Write(util.EncodeCertsPEM(cert, caCerts))
 		resp.Write(keyBytes)
 	})
 }
diff --git a/pkg/util/cert.go b/pkg/util/cert.go
new file mode 100644
index 000000000000..bad59d8d9a4f
--- /dev/null
+++ b/pkg/util/cert.go
@@ -0,0 +1,17 @@
+package util
+
+import (
+	"crypto/x509"
+
+	certutil "github.com/rancher/dynamiclistener/cert"
+)
+
+// EncodeCertsPEM is a wrapper around the EncodeCertPEM function to return the
+// PEM encoding of a cert and chain, instead of just a single cert.
+func EncodeCertsPEM(cert *x509.Certificate, caCerts []*x509.Certificate) []byte {
+	pemBytes := certutil.EncodeCertPEM(cert)
+	for _, caCert := range caCerts {
+		pemBytes = append(pemBytes, certutil.EncodeCertPEM(caCert)...)
+	}
+	return pemBytes
+}