diff --git a/CHANGELOG.md b/CHANGELOG.md
index addd73600a6..9dd17909559 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -15,6 +15,7 @@ IMPROVEMENTS:
 
 
 BUG FIXES:
+ * core: Fix treating valid PEM files as invalid [[GH-4613](https://github.com/hashicorp/nomad/issues/4613)]
  * core: Reset queued allocation summary to zero when job stopped [[GH-4414](https://github.com/hashicorp/nomad/issues/4414)]
  * core: Fix panic due to missing synchronization in delayed evaluations heap [[GH-4632](https://github.com/hashicorp/nomad/issues/4632)]
  * client: Fix migrating ephemeral disks when TLS is enabled [[GH-4648](https://github.com/hashicorp/nomad/issues/4648)]
diff --git a/helper/tlsutil/config.go b/helper/tlsutil/config.go
index 707ed59299c..820ac92f1ba 100644
--- a/helper/tlsutil/config.go
+++ b/helper/tlsutil/config.go
@@ -5,7 +5,6 @@ import (
 	"crypto/rsa"
 	"crypto/tls"
 	"crypto/x509"
-	"encoding/pem"
 	"fmt"
 	"io/ioutil"
 	"net"
@@ -194,35 +193,11 @@ func (c *Config) AppendCA(pool *x509.CertPool) error {
 		return fmt.Errorf("Failed to read CA file: %v", err)
 	}
 
-	block, rest := pem.Decode(data)
-	if err := validateCertificate(block); err != nil {
-		return err
-	}
-
-	for len(rest) > 0 {
-		block, rest = pem.Decode(rest)
-		if err := validateCertificate(block); err != nil {
-			return err
-		}
-	}
-
+	// Read certificates and return an error if no valid certificates were
+	// found. Unfortunately it is very difficult to return meaningful
+	// errors as PEM files are extremely permissive.
 	if !pool.AppendCertsFromPEM(data) {
-		return fmt.Errorf("Failed to add any CA certificates")
-	}
-
-	return nil
-}
-
-// validateCertificate checks to ensure a certificate is valid. If it is not,
-// return a descriptive error of why the certificate is invalid.
-func validateCertificate(block *pem.Block) error {
-	if block == nil {
-		return fmt.Errorf("Failed to decode CA file from pem format")
-	}
-
-	// Parse the certificate to ensure that it is properly formatted
-	if _, err := x509.ParseCertificates(block.Bytes); err != nil {
-		return fmt.Errorf("Failed to parse CA file: %v", err)
+		return fmt.Errorf("Failed to parse any valid certificates in CA file: %s", c.CAFile)
 	}
 
 	return nil
diff --git a/helper/tlsutil/config_test.go b/helper/tlsutil/config_test.go
index 249b6470e6a..f1837db7bde 100644
--- a/helper/tlsutil/config_test.go
+++ b/helper/tlsutil/config_test.go
@@ -51,10 +51,6 @@ func TestConfig_AppendCA_Valid(t *testing.T) {
 func TestConfig_AppendCA_Valid_MultipleCerts(t *testing.T) {
 	require := require.New(t)
 
-	tmpCAFile, err := ioutil.TempFile("/tmp", "test_ca_file")
-	require.Nil(err)
-	defer os.Remove(tmpCAFile.Name())
-
 	certs := `
 -----BEGIN CERTIFICATE-----
 MIICMzCCAdqgAwIBAgIUNZ9L86Xp9EuDH0/qyAesh599LXQwCgYIKoZIzj0EAwIw
@@ -71,6 +67,61 @@ AQYwDwYDVR0TAQH/BAUwAwEB/zAdBgNVHQ4EFgQUOjVq/BectnhcKn6EHUD4NJFm
 Ln2ZUe8CIDsQswBQS7URbqnKYDye2Y4befJkr4fmhhmMQb2ex9A4
 -----END CERTIFICATE-----
 -----BEGIN CERTIFICATE-----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+-----END CERTIFICATE-----
+`
+
+	tmpCAFile, err := ioutil.TempFile("/tmp", "test_ca_file")
+	require.NoError(err)
+	defer os.Remove(tmpCAFile.Name())
+
+	_, err = tmpCAFile.Write([]byte(certs))
+	require.NoError(err)
+	tmpCAFile.Close()
+
+	conf := &Config{
+		CAFile: tmpCAFile.Name(),
+	}
+	pool := x509.NewCertPool()
+	require.NoError(conf.AppendCA(pool))
+
+	require.Len(pool.Subjects(), 2)
+}
+
+// TestConfig_AppendCA_Valid_Whitespace asserts that a PEM file containing
+// trailing whitespace is valid.
+func TestConfig_AppendCA_Valid_Whitespace(t *testing.T) {
+	require := require.New(t)
+
+	const cacertWhitespace = "./testdata/ca-whitespace.pem"
+	conf := &Config{
+		CAFile: cacertWhitespace,
+	}
+	pool := x509.NewCertPool()
+	require.NoError(conf.AppendCA(pool))
+
+	require.Len(pool.Subjects(), 1)
+}
+
+// TestConfig_AppendCA_Invalid_MultipleCerts_Whitespace asserts that a PEM file
+// containing non-PEM data between certificate blocks is still valid.
+func TestConfig_AppendCA_Valid_MultipleCerts_ExtraData(t *testing.T) {
+	require := require.New(t)
+
+	certs := `
+Did you know...
+-----BEGIN CERTIFICATE-----
 MIICMzCCAdqgAwIBAgIUNZ9L86Xp9EuDH0/qyAesh599LXQwCgYIKoZIzj0EAwIw
 eDELMAkGA1UEBhMCVVMxEzARBgNVBAgTCkNhbGlmb3JuaWExFjAUBgNVBAcTDVNh
 biBGcmFuY2lzY28xEjAQBgNVBAoTCUhhc2hpQ29ycDEOMAwGA1UECxMFTm9tYWQx
@@ -83,10 +134,34 @@ uNdZJZWSi4Q/4HojM5FTSBqYxNgSrmY/o3oQrCPlo0IwQDAOBgNVHQ8BAf8EBAMC
 AQYwDwYDVR0TAQH/BAUwAwEB/zAdBgNVHQ4EFgQUOjVq/BectnhcKn6EHUD4NJFm
 /UAwCgYIKoZIzj0EAwIDRwAwRAIgTemDJGSGtcQPXLWKiQNw4SKO9wAPhn/WoKW4
 Ln2ZUe8CIDsQswBQS7URbqnKYDye2Y4befJkr4fmhhmMQb2ex9A4
------END CERTIFICATE-----`
+-----END CERTIFICATE-----
+
+...PEM parsers don't care about data...
+
+-----BEGIN CERTIFICATE-----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+-----END CERTIFICATE-----
+
+...outside of -----XXX----- blocks?
+`
 
+	tmpCAFile, err := ioutil.TempFile("/tmp", "test_ca_file_extra")
+	require.NoError(err)
+	defer os.Remove(tmpCAFile.Name())
 	_, err = tmpCAFile.Write([]byte(certs))
-	require.Nil(err)
+	require.NoError(err)
+	tmpCAFile.Close()
 
 	conf := &Config{
 		CAFile: tmpCAFile.Name(),
@@ -94,16 +169,15 @@ Ln2ZUe8CIDsQswBQS7URbqnKYDye2Y4befJkr4fmhhmMQb2ex9A4
 	pool := x509.NewCertPool()
 	err = conf.AppendCA(pool)
 
-	require.Nil(err)
+	require.NoError(err)
+	require.Len(pool.Subjects(), 2)
 }
 
-func TestConfig_AppendCA_InValid_MultipleCerts(t *testing.T) {
+// TestConfig_AppendCA_Invalid_MultipleCerts asserts only the valid certificate
+// is returned.
+func TestConfig_AppendCA_Invalid_MultipleCerts(t *testing.T) {
 	require := require.New(t)
 
-	tmpCAFile, err := ioutil.TempFile("/tmp", "test_ca_file")
-	require.Nil(err)
-	defer os.Remove(tmpCAFile.Name())
-
 	certs := `
 -----BEGIN CERTIFICATE-----
 MIICMzCCAdqgAwIBAgIUNZ9L86Xp9EuDH0/qyAesh599LXQwCgYIKoZIzj0EAwIw
@@ -123,16 +197,20 @@ Ln2ZUe8CIDsQswBQS7URbqnKYDye2Y4befJkr4fmhhmMQb2ex9A4
 Invalid
 -----END CERTIFICATE-----`
 
+	tmpCAFile, err := ioutil.TempFile("/tmp", "test_ca_file")
+	require.NoError(err)
+	defer os.Remove(tmpCAFile.Name())
 	_, err = tmpCAFile.Write([]byte(certs))
-	require.Nil(err)
+	require.NoError(err)
+	tmpCAFile.Close()
 
 	conf := &Config{
 		CAFile: tmpCAFile.Name(),
 	}
 	pool := x509.NewCertPool()
-	err = conf.AppendCA(pool)
+	require.NoError(conf.AppendCA(pool))
 
-	require.NotNil(err)
+	require.Len(pool.Subjects(), 1)
 }
 
 func TestConfig_AppendCA_Invalid(t *testing.T) {
@@ -160,8 +238,8 @@ func TestConfig_AppendCA_Invalid(t *testing.T) {
 		}
 		pool := x509.NewCertPool()
 		err = conf.AppendCA(pool)
-		require.NotNil(err)
-		require.Contains(err.Error(), "Failed to decode CA file from pem format")
+		require.Error(err)
+		require.Contains(err.Error(), "Failed to parse any valid certificates in CA file:")
 		require.Equal(len(pool.Subjects()), 0)
 	}
 }
diff --git a/helper/tlsutil/testdata/ca-whitespace.pem b/helper/tlsutil/testdata/ca-whitespace.pem
new file mode 100644
index 00000000000..a8a7a189143
--- /dev/null
+++ b/helper/tlsutil/testdata/ca-whitespace.pem
@@ -0,0 +1,15 @@
+-----BEGIN CERTIFICATE-----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+-----END CERTIFICATE-----
+