diff --git a/lib/srv/alpnproxy/local_proxy.go b/lib/srv/alpnproxy/local_proxy.go
index 813ae59e7c0a8..26157fab19389 100644
--- a/lib/srv/alpnproxy/local_proxy.go
+++ b/lib/srv/alpnproxy/local_proxy.go
@@ -314,6 +314,8 @@ func (l *LocalProxy) StartHTTPAccessProxy(ctx context.Context) error {
 		// localhost. Set appropriate header to keep this information.
 		if addr, err := utils.ParseAddr(req.Host); err == nil && !addr.IsLocal() {
 			req.Header.Set("X-Forwarded-Host", req.Host)
+		} else { // ensure that there is no client provided X-Forwarded-Host
+			req.Header.Del("X-Forwarded-Host")
 		}
 
 		proxy, err := l.getHTTPReverseProxyForReq(req, defaultProxy)
diff --git a/lib/srv/app/aws/endpoints.go b/lib/srv/app/aws/endpoints.go
index e1032df3e011b..b6f4122780c25 100644
--- a/lib/srv/app/aws/endpoints.go
+++ b/lib/srv/app/aws/endpoints.go
@@ -53,6 +53,7 @@ import (
 	"github.com/gravitational/trace"
 
 	awsapiutils "github.com/gravitational/teleport/api/utils/aws"
+	libutils "github.com/gravitational/teleport/lib/utils"
 	awsutils "github.com/gravitational/teleport/lib/utils/aws"
 )
 
@@ -61,7 +62,8 @@ import (
 // endpoint.
 func resolveEndpoint(r *http.Request) (*endpoints.ResolvedEndpoint, error) {
 	// Use X-Forwarded-Host header if it is a valid AWS endpoint.
-	if awsapiutils.IsAWSEndpoint(r.Header.Get("X-Forwarded-Host")) {
+	forwardedHost, headErr := libutils.GetSingleHeader(r.Header, "X-Forwarded-Host")
+	if headErr == nil && awsapiutils.IsAWSEndpoint(forwardedHost) {
 		re, err := resolveEndpointByXForwardedHost(r, awsutils.AuthorizationHeader)
 		return re, trace.Wrap(err)
 	}
diff --git a/lib/srv/app/azure/handler.go b/lib/srv/app/azure/handler.go
index 7811106a73b87..159d0d864d9e4 100644
--- a/lib/srv/app/azure/handler.go
+++ b/lib/srv/app/azure/handler.go
@@ -167,8 +167,10 @@ func (s *handler) formatForwardResponseError(rw http.ResponseWriter, r *http.Req
 
 // prepareForwardRequest prepares a request for forwarding, updating headers and target host. Several checks are made along the way.
 func (s *handler) prepareForwardRequest(r *http.Request, sessionCtx *common.SessionContext) (*http.Request, error) {
-	forwardedHost := r.Header.Get("X-Forwarded-Host")
-	if !azure.IsAzureEndpoint(forwardedHost) {
+	forwardedHost, err := utils.GetSingleHeader(r.Header, "X-Forwarded-Host")
+	if err != nil {
+		return nil, trace.AccessDenied(err.Error())
+	} else if !azure.IsAzureEndpoint(forwardedHost) {
 		return nil, trace.AccessDenied("%q is not an Azure endpoint", forwardedHost)
 	}
 
diff --git a/lib/srv/app/gcp/handler.go b/lib/srv/app/gcp/handler.go
index 3ca604556ce74..4b687ca8d3917 100644
--- a/lib/srv/app/gcp/handler.go
+++ b/lib/srv/app/gcp/handler.go
@@ -191,8 +191,10 @@ func (s *handler) formatForwardResponseError(rw http.ResponseWriter, r *http.Req
 
 // prepareForwardRequest prepares a request for forwarding, updating headers and target host. Several checks are made along the way.
 func (s *handler) prepareForwardRequest(r *http.Request, sessionCtx *common.SessionContext) (*http.Request, error) {
-	forwardedHost := r.Header.Get("X-Forwarded-Host")
-	if !gcp.IsGCPEndpoint(forwardedHost) {
+	forwardedHost, err := utils.GetSingleHeader(r.Header, "X-Forwarded-Host")
+	if err != nil {
+		return nil, trace.AccessDenied(err.Error())
+	} else if !gcp.IsGCPEndpoint(forwardedHost) {
 		return nil, trace.AccessDenied("%q is not a GCP endpoint", forwardedHost)
 	}
 
diff --git a/lib/utils/http.go b/lib/utils/http.go
index fae574b37e503..e0717bf170c54 100644
--- a/lib/utils/http.go
+++ b/lib/utils/http.go
@@ -117,6 +117,19 @@ func GetAnyHeader(header http.Header, keys ...string) string {
 	return ""
 }
 
+// GetSingleHeader will return the header value for the key if there is exactly one value present.  If the header is
+// missing or specified multiple times, an error will be returned.
+func GetSingleHeader(headers http.Header, key string) (string, error) {
+	values := headers.Values(key)
+	if len(values) > 1 {
+		return "", trace.BadParameter("multiple %q headers", key)
+	} else if len(values) == 0 {
+		return "", trace.NotFound("missing %q headers", key)
+	} else {
+		return values[0], nil
+	}
+}
+
 // HTTPDoClient is an interface that defines the Do function of http.Client.
 type HTTPDoClient interface {
 	Do(req *http.Request) (*http.Response, error)
diff --git a/lib/utils/http_test.go b/lib/utils/http_test.go
index df9b0b9cb1c0b..bf5d57a328468 100644
--- a/lib/utils/http_test.go
+++ b/lib/utils/http_test.go
@@ -20,6 +20,7 @@ import (
 	"io"
 	"net/http"
 	"net/http/httptest"
+	"strings"
 	"testing"
 
 	"github.com/stretchr/testify/require"
@@ -54,6 +55,52 @@ func TestGetAnyHeader(t *testing.T) {
 	require.Equal(t, "b1", GetAnyHeader(header, "bbb", "aaa"))
 }
 
+func TestGetSingleHeader(t *testing.T) {
+	t.Run("NoValue", func(t *testing.T) {
+		t.Parallel()
+		headers := make(http.Header)
+
+		result, err := GetSingleHeader(headers, "key")
+		require.Empty(t, result)
+		require.Error(t, err)
+	})
+	t.Run("SingleValue", func(t *testing.T) {
+		t.Parallel()
+		headers := make(http.Header)
+		key := "key"
+		value := "value"
+		headers.Set(key, value)
+
+		result, err := GetSingleHeader(headers, key)
+		require.NoError(t, err)
+		require.Equal(t, value, result)
+	})
+	t.Run("DuplicateValue", func(t *testing.T) {
+		t.Parallel()
+		headers := make(http.Header)
+		key := "key"
+		value := "value1"
+		headers.Add(key, value)
+		headers.Add(key, "value2")
+
+		result, err := GetSingleHeader(headers, key)
+		require.Empty(t, result)
+		require.Error(t, err)
+	})
+	t.Run("DuplicateCaseValue", func(t *testing.T) {
+		t.Parallel()
+		headers := make(http.Header)
+		key := "key"
+		value := "value1"
+		headers.Add(key, value)
+		headers.Add(strings.ToUpper(key), "value2")
+
+		result, err := GetSingleHeader(headers, key)
+		require.Empty(t, result)
+		require.Error(t, err)
+	})
+}
+
 func TestChainHTTPMiddlewares(t *testing.T) {
 	baseHandler := http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
 		w.Write([]byte("baseHandler"))