diff --git a/api/client/proxy/proxy.go b/api/client/proxy/proxy.go
index 7b95b3ba8a4df..c1e3da4322c46 100644
--- a/api/client/proxy/proxy.go
+++ b/api/client/proxy/proxy.go
@@ -71,32 +71,39 @@ func parse(addr string) (*url.URL, error) {
 	return addrURL, nil
 }
 
-// HTTPFallbackRoundTripper is a wrapper for http.Transport that downgrades requests
-// to plain HTTP when using a plain HTTP proxy at localhost.
-type HTTPFallbackRoundTripper struct {
+// HTTPRoundTripper is a wrapper for http.Transport that
+// - adds extra HTTP headers to all requests, and
+// - downgrades requests to plain HTTP when proxy is at localhost and the wrapped http.Transport has TLSClientConfig.InsecureSkipVerify set to true.
+type HTTPRoundTripper struct {
 	*http.Transport
+	// extraHeaders is a map of extra HTTP headers to be included in requests.
+	extraHeaders map[string]string
+	// isProxyHTTPLocalhost indicates that the HTTP_PROXY is at "http://localhost"
 	isProxyHTTPLocalhost bool
 }
 
-// NewHTTPFallbackRoundTripper creates a new initialized HTTP fallback roundtripper.
-func NewHTTPFallbackRoundTripper(transport *http.Transport, insecure bool) *HTTPFallbackRoundTripper {
+// NewHTTPRoundTripper creates a new initialized HTTP roundtripper.
+func NewHTTPRoundTripper(transport *http.Transport, extraHeaders map[string]string) *HTTPRoundTripper {
 	proxyConfig := httpproxy.FromEnvironment()
-	rt := HTTPFallbackRoundTripper{
+	return &HTTPRoundTripper{
 		Transport:            transport,
+		extraHeaders:         extraHeaders,
 		isProxyHTTPLocalhost: strings.HasPrefix(proxyConfig.HTTPProxy, "http://localhost"),
 	}
-	if rt.TLSClientConfig != nil {
-		rt.TLSClientConfig.InsecureSkipVerify = insecure
-	}
-	return &rt
 }
 
 // RoundTrip executes a single HTTP transaction. Part of the RoundTripper interface.
-func (rt *HTTPFallbackRoundTripper) RoundTrip(req *http.Request) (*http.Response, error) {
-	tlsConfig := rt.Transport.TLSClientConfig
+func (rt *HTTPRoundTripper) RoundTrip(req *http.Request) (*http.Response, error) {
+	// Add extra HTTP headers.
+	for header, v := range rt.extraHeaders {
+		req.Header.Add(header, v)
+	}
+
 	// Use plain HTTP if proxying via http://localhost in insecure mode.
+	tlsConfig := rt.Transport.TLSClientConfig
 	if rt.isProxyHTTPLocalhost && tlsConfig != nil && tlsConfig.InsecureSkipVerify {
 		req.URL.Scheme = "http"
 	}
+
 	return rt.Transport.RoundTrip(req)
 }
diff --git a/api/client/proxy/proxy_test.go b/api/client/proxy/proxy_test.go
index 08f05bfbe9f3a..939b530f91865 100644
--- a/api/client/proxy/proxy_test.go
+++ b/api/client/proxy/proxy_test.go
@@ -19,7 +19,9 @@ package proxy
 import (
 	"crypto/tls"
 	"fmt"
+	"net"
 	"net/http"
+	"net/http/httptest"
 	"net/url"
 	"strings"
 	"testing"
@@ -182,12 +184,14 @@ func buildProxyAddr(addr, user, pass string) (string, error) {
 func TestProxyAwareRoundTripper(t *testing.T) {
 	t.Setenv("HTTP_PROXY", "http://localhost:8888")
 	transport := &http.Transport{
-		TLSClientConfig: &tls.Config{},
+		TLSClientConfig: &tls.Config{
+			InsecureSkipVerify: true,
+		},
 		Proxy: func(req *http.Request) (*url.URL, error) {
 			return httpproxy.FromEnvironment().ProxyFunc()(req.URL)
 		},
 	}
-	rt := NewHTTPFallbackRoundTripper(transport, true)
+	rt := NewHTTPRoundTripper(transport, nil)
 	req, err := http.NewRequest(http.MethodGet, "https://localhost:9999", nil)
 	require.NoError(t, err)
 	// Don't care about response, only if the scheme changed.
@@ -197,6 +201,190 @@ func TestProxyAwareRoundTripper(t *testing.T) {
 	require.Equal(t, "http", req.URL.Scheme)
 }
 
+// TestHttpRoundTripperDowngrade tests that the round tripper downgrades https requests to http
+// when HTTP_PROXY is set to "http://localhost:*" (i.e. there's an http proxy running on localhost).
+func TestHttpRoundTripperDowngrade(t *testing.T) {
+	testCases := []struct {
+		desc           string
+		setHTTPProxy   bool
+		shouldHitProxy bool
+	}{
+		{
+			desc:           "hits http proxy if insecure and localhost http proxy is set",
+			setHTTPProxy:   true,
+			shouldHitProxy: true,
+		},
+		{
+			desc:           "does not hit http proxy if insecure and localhost http proxy is not set",
+			setHTTPProxy:   false,
+			shouldHitProxy: false,
+		},
+	}
+
+	for _, tc := range testCases {
+		t.Run(tc.desc, func(t *testing.T) {
+			newHandler := func(runningAtProxy bool, wasHit *bool) http.HandlerFunc {
+				return func(w http.ResponseWriter, r *http.Request) {
+					*wasHit = true
+					if tc.shouldHitProxy {
+						// If the request should hit the proxy, then:
+						// - this handler is running at the proxy, and
+						// - the scheme should be http.
+						require.True(t, runningAtProxy)
+						require.Equal(t, "http", r.URL.Scheme)
+					}
+					w.WriteHeader(http.StatusOK)
+				}
+			}
+
+			// Start localhost http proxy.
+			runningAtProxy := true
+			loopback := true
+			https := false
+			httpProxyWasHit := false
+			httpProxy, err := newServer(newHandler(runningAtProxy, &httpProxyWasHit), loopback, https)
+			require.NoError(t, err)
+			defer httpProxy.Close()
+
+			// Start non-localhost https server.
+			runningAtProxy = false
+			loopback = false
+			https = true
+			httpsSrvWasHit := false
+			httpsSrv, err := newServer(newHandler(runningAtProxy, &httpsSrvWasHit), loopback, https)
+			require.NoError(t, err)
+			defer httpsSrv.Close()
+
+			if tc.setHTTPProxy {
+				// url.Parse won't correctly parse an absolute URL without a scheme.
+				u, err := url.Parse("http://" + httpProxy.Listener.Addr().String())
+				require.NoError(t, err)
+				_, port, err := net.SplitHostPort(u.Host)
+				require.NoError(t, err)
+
+				// Set HTTP_PROXY to "http://localhost:*".
+				t.Setenv("HTTP_PROXY", fmt.Sprintf("http://localhost:%s", port))
+			}
+
+			clt := newClient(t, nil)
+
+			// Perform any request.
+			// Set addr to the https server. If HTTP_PROXY was set above,
+			// the http proxy should be hit regardless.
+			addr := httpsSrv.Listener.Addr().String()
+			request(t, clt, addr)
+
+			// Validate that the correct server was hit.
+			require.Equal(t, tc.shouldHitProxy, httpProxyWasHit)
+			require.Equal(t, !tc.shouldHitProxy, httpsSrvWasHit)
+		})
+	}
+}
+
+// TestHttpRoundTripperExtraHeaders tests that the round tripper adds the extra headers set.
+func TestHttpRoundTripperExtraHeaders(t *testing.T) {
+	testCases := []struct {
+		desc          string
+		extraHeaders  map[string]string
+		expectHeaders func(*testing.T, http.Header)
+	}{
+		{
+			desc: "extra headers are added",
+			extraHeaders: map[string]string{
+				"header1": "value1",
+				"header2": "value2",
+			},
+			expectHeaders: func(t *testing.T, headers http.Header) {
+				require.Equal(t, []string{"value1"}, headers.Values("header1"))
+				require.Equal(t, []string{"value2"}, headers.Values("header2"))
+			},
+		},
+		{
+			desc: "extra headers do not overwrite existing headers",
+			extraHeaders: map[string]string{
+				"header1":      "value1",
+				"Content-Type": "value2",
+			},
+			expectHeaders: func(t *testing.T, headers http.Header) {
+				require.Equal(t, []string{"value1"}, headers.Values("header1"))
+				require.Equal(t, []string{"application/json", "value2"}, headers.Values("Content-Type"))
+			},
+		},
+	}
+
+	for _, tc := range testCases {
+		t.Run(tc.desc, func(t *testing.T) {
+			var handler http.HandlerFunc = func(w http.ResponseWriter, r *http.Request) {
+				tc.expectHeaders(t, r.Header)
+				w.WriteHeader(http.StatusOK)
+			}
+
+			// Start localhost https server.
+			loopback := true
+			tls := true
+			httpsSrv, err := newServer(handler, loopback, tls)
+			require.NoError(t, err)
+			defer httpsSrv.Close()
+
+			clt := newClient(t, tc.extraHeaders)
+
+			// Perform any request.
+			// Set the address to the localhost https server.
+			addr := httpsSrv.Listener.Addr().String()
+			request(t, clt, addr)
+		})
+	}
+}
+
+// newServer starts a new server that:
+// - runs TLS if `https`
+// - uses a loopback listener if `loopback`
+func newServer(handler http.HandlerFunc, loopback bool, https bool) (*httptest.Server, error) {
+	srv := httptest.NewUnstartedServer(handler)
+
+	if !loopback {
+		// Replace the test-supplied loopback listener with the first available
+		// non-loopback address.
+		srv.Listener.Close()
+		l, err := net.Listen("tcp", "0.0.0.0:0")
+		if err != nil {
+			return nil, err
+		}
+		srv.Listener = l
+	}
+
+	if https {
+		srv.StartTLS()
+	} else {
+		srv.Start()
+	}
+	return srv, nil
+}
+
+// newClient creates a new https roundtrip client.
+func newClient(t *testing.T, extraHeaders map[string]string) *http.Client {
+	transport := &http.Transport{
+		TLSClientConfig: &tls.Config{
+			// Setting insecure ensures that https requests succeed.
+			InsecureSkipVerify: true,
+		},
+		Proxy: func(req *http.Request) (*url.URL, error) {
+			return httpproxy.FromEnvironment().ProxyFunc()(req.URL)
+		},
+	}
+	return &http.Client{
+		Transport: NewHTTPRoundTripper(transport, extraHeaders),
+	}
+}
+
+// request perform a POST request.
+func request(t *testing.T, clt *http.Client, addr string) {
+	url := "https://" + addr + "/v1/content"
+	resp, err := clt.Post(url, "application/json", nil)
+	require.NoError(t, err)
+	require.NoError(t, resp.Body.Close())
+}
+
 func TestParse(t *testing.T) {
 	successTests := []struct {
 		name, addr, scheme, host, path string
diff --git a/api/client/webclient/webclient.go b/api/client/webclient/webclient.go
index 771390111a5fb..505c8648b3372 100644
--- a/api/client/webclient/webclient.go
+++ b/api/client/webclient/webclient.go
@@ -103,7 +103,7 @@ func newWebClient(cfg *Config) (*http.Client, error) {
 	}
 	return &http.Client{
 		Transport: otelhttp.NewTransport(
-			proxy.NewHTTPFallbackRoundTripper(&transport, cfg.Insecure),
+			proxy.NewHTTPRoundTripper(&transport, nil),
 			otelhttp.WithSpanNameFormatter(tracing.HTTPTransportFormatter),
 		),
 		Timeout: cfg.Timeout,
diff --git a/lib/client/api.go b/lib/client/api.go
index b2e4495db876b..5002195388abf 100644
--- a/lib/client/api.go
+++ b/lib/client/api.go
@@ -2787,7 +2787,12 @@ func makeProxySSHClient(ctx context.Context, tc *TeleportClient, sshConfig *ssh.
 	if len(tc.JumpHosts) > 0 {
 		sshProxyAddr = tc.JumpHosts[0].Addr.Addr
 		// Check if JumpHost address is a proxy web address.
-		resp, err := webclient.Find(&webclient.Config{Context: ctx, ProxyAddr: sshProxyAddr, Insecure: tc.InsecureSkipVerify})
+		resp, err := webclient.Find(&webclient.Config{
+			Context:      ctx,
+			ProxyAddr:    sshProxyAddr,
+			Insecure:     tc.InsecureSkipVerify,
+			ExtraHeaders: tc.ExtraProxyHeaders,
+		})
 		// If JumpHost address is a proxy web port and proxy supports TLSRouting dial proxy with TLSWrapper.
 		if err == nil && resp.Proxy.TLSRoutingEnabled {
 			log.Infof("Connecting to proxy=%v login=%q using TLS Routing JumpHost", sshProxyAddr, sshConfig.User)
@@ -3284,6 +3289,7 @@ func (tc *TeleportClient) newSSHLogin(priv *keys.PrivateKey) (SSHLogin, error) {
 		RouteToCluster:       tc.SiteName,
 		KubernetesCluster:    tc.KubernetesCluster,
 		AttestationStatement: attestationStatement,
+		ExtraHeaders:         tc.ExtraProxyHeaders,
 	}, nil
 }
 
diff --git a/lib/client/https_client.go b/lib/client/https_client.go
index 4e7f4c8e43e08..5c2f0ebf0bddb 100644
--- a/lib/client/https_client.go
+++ b/lib/client/https_client.go
@@ -37,39 +37,30 @@ import (
 )
 
 func NewInsecureWebClient() *http.Client {
-	// Because Teleport clients can't be configured (yet), they take the default
-	// list of cipher suites from Go.
-	tlsConfig := utils.TLSConfig(nil)
-	transport := http.Transport{
-		TLSClientConfig: tlsConfig,
-		Proxy: func(req *http.Request) (*url.URL, error) {
-			return httpproxy.FromEnvironment().ProxyFunc()(req.URL)
-		},
-	}
+	return newClient(true, nil, nil)
+}
+
+func newClient(insecure bool, pool *x509.CertPool, extraHeaders map[string]string) *http.Client {
 	return &http.Client{
 		Transport: otelhttp.NewTransport(
-			apiproxy.NewHTTPFallbackRoundTripper(&transport, true /* insecure */),
+			apiproxy.NewHTTPRoundTripper(httpTransport(insecure, pool), extraHeaders),
 			otelhttp.WithSpanNameFormatter(tracing.HTTPTransportFormatter),
 		),
 	}
 }
 
-func newClientWithPool(pool *x509.CertPool) *http.Client {
+func httpTransport(insecure bool, pool *x509.CertPool) *http.Transport {
 	// Because Teleport clients can't be configured (yet), they take the default
 	// list of cipher suites from Go.
 	tlsConfig := utils.TLSConfig(nil)
+	tlsConfig.InsecureSkipVerify = insecure
 	tlsConfig.RootCAs = pool
 
-	return &http.Client{
-		Transport: otelhttp.NewTransport(
-			&http.Transport{
-				TLSClientConfig: tlsConfig,
-				Proxy: func(req *http.Request) (*url.URL, error) {
-					return httpproxy.FromEnvironment().ProxyFunc()(req.URL)
-				},
-			},
-			otelhttp.WithSpanNameFormatter(tracing.HTTPTransportFormatter),
-		),
+	return &http.Transport{
+		TLSClientConfig: tlsConfig,
+		Proxy: func(req *http.Request) (*url.URL, error) {
+			return httpproxy.FromEnvironment().ProxyFunc()(req.URL)
+		},
 	}
 }
 
diff --git a/lib/client/https_client_test.go b/lib/client/https_client_test.go
index 7482df7fd0ea8..c37ad5207610a 100644
--- a/lib/client/https_client_test.go
+++ b/lib/client/https_client_test.go
@@ -46,9 +46,9 @@ func TestNewInsecureWebClientNoProxy(t *testing.T) {
 	require.Contains(t, err.Error(), "no such host")
 }
 
-func TestNewClientWithPoolHTTPProxy(t *testing.T) {
+func TestNewSecureWebClientHTTPProxy(t *testing.T) {
 	t.Setenv("HTTPS_PROXY", "fakeproxy.example.com:9999")
-	client := newClientWithPool(nil)
+	client := newClient(false, nil, nil)
 	//nolint:bodyclose // resp should be nil, so there will be no body to close.
 	resp, err := client.Get("https://fakedomain.example.com")
 	// Client should try to proxy through nonexistent server at localhost.
@@ -58,10 +58,10 @@ func TestNewClientWithPoolHTTPProxy(t *testing.T) {
 	require.Contains(t, err.Error(), "no such host")
 }
 
-func TestNewClientWithPoolNoProxy(t *testing.T) {
+func TestNewSecureWebClientNoProxy(t *testing.T) {
 	t.Setenv("HTTPS_PROXY", "fakeproxy.example.com:9999")
 	t.Setenv("NO_PROXY", "fakedomain.example.com")
-	client := newClientWithPool(nil)
+	client := newClient(false, nil, nil)
 	//nolint:bodyclose // resp should be nil, so there will be no body to close.
 	resp, err := client.Get("https://fakedomain.example.com")
 	require.Error(t, err, "GET unexpectedly succeeded: %+v", resp)
diff --git a/lib/client/redirect.go b/lib/client/redirect.go
index 419d69ff0bb2a..cb92e5206e24a 100644
--- a/lib/client/redirect.go
+++ b/lib/client/redirect.go
@@ -91,7 +91,7 @@ type RedirectorConfig struct {
 
 // NewRedirector returns new local web server redirector
 func NewRedirector(ctx context.Context, login SSHLoginSSO, config *RedirectorConfig) (*Redirector, error) {
-	clt, proxyURL, err := initClient(login.ProxyAddr, login.Insecure, login.Pool)
+	clt, proxyURL, err := initClient(login.ProxyAddr, login.Insecure, login.Pool, login.ExtraHeaders)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
diff --git a/lib/client/weblogin.go b/lib/client/weblogin.go
index 51687be3e5173..aa347516d1af5 100644
--- a/lib/client/weblogin.go
+++ b/lib/client/weblogin.go
@@ -172,7 +172,7 @@ type SSHLogin struct {
 	TTL time.Duration
 	// Insecure turns off verification for x509 target proxy
 	Insecure bool
-	// Pool is x509 cert pool to use for server certifcate verification
+	// Pool is x509 cert pool to use for server certificate verification
 	Pool *x509.CertPool
 	// Compatibility sets compatibility mode for SSH certificates
 	Compatibility string
@@ -184,6 +184,8 @@ type SSHLogin struct {
 	KubernetesCluster string
 	// AttestationStatement is an attestation statement.
 	AttestationStatement *keys.AttestationStatement
+	// ExtraHeaders is a map of extra HTTP headers to be included in requests.
+	ExtraHeaders map[string]string
 }
 
 // SSHLoginSSO contains SSH login parameters for SSO login.
@@ -250,13 +252,13 @@ type SSHLoginPasswordless struct {
 }
 
 // initClient creates a new client to the HTTPS web proxy.
-func initClient(proxyAddr string, insecure bool, pool *x509.CertPool) (*WebClient, *url.URL, error) {
+func initClient(proxyAddr string, insecure bool, pool *x509.CertPool, extraHeaders map[string]string) (*WebClient, *url.URL, error) {
 	log := logrus.WithFields(logrus.Fields{
 		trace.Component: teleport.ComponentClient,
 	})
-	log.Debugf("HTTPS client init(proxyAddr=%v, insecure=%v)", proxyAddr, insecure)
+	log.Debugf("HTTPS client init(proxyAddr=%v, insecure=%v, extraHeaders=%v)", proxyAddr, insecure, extraHeaders)
 
-	// validate proxyAddr:
+	// validate proxy address
 	host, port, err := net.SplitHostPort(proxyAddr)
 	if err != nil || host == "" || port == "" {
 		if err != nil {
@@ -270,18 +272,13 @@ func initClient(proxyAddr string, insecure bool, pool *x509.CertPool) (*WebClien
 		return nil, nil, trace.BadParameter("'%v' is not a valid proxy address", proxyAddr)
 	}
 
-	var opts []roundtrip.ClientParam
-
 	if insecure {
-		// Skip https cert verification, print a warning that this is insecure.
+		// Skipping https cert verification, print a warning that this is insecure.
 		fmt.Fprintf(os.Stderr, "WARNING: You are using insecure connection to Teleport proxy %v\n", proxyAddr)
-		opts = append(opts, roundtrip.HTTPClient(NewInsecureWebClient()))
-	} else if pool != nil {
-		// use custom set of trusted CAs
-		opts = append(opts, roundtrip.HTTPClient(newClientWithPool(pool)))
 	}
 
-	clt, err := NewWebClient(proxyAddr, opts...)
+	opt := roundtrip.HTTPClient(newClient(insecure, pool, extraHeaders))
+	clt, err := NewWebClient(proxyAddr, opt)
 	if err != nil {
 		return nil, nil, trace.Wrap(err)
 	}
@@ -360,7 +357,7 @@ func SSHAgentSSOLogin(ctx context.Context, login SSHLoginSSO, config *Redirector
 
 // SSHAgentLogin is used by tsh to fetch local user credentials.
 func SSHAgentLogin(ctx context.Context, login SSHLoginDirect) (*auth.SSHLoginResponse, error) {
-	clt, _, err := initClient(login.ProxyAddr, login.Insecure, login.Pool)
+	clt, _, err := initClient(login.ProxyAddr, login.Insecure, login.Pool, login.ExtraHeaders)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
@@ -395,7 +392,7 @@ func SSHAgentLogin(ctx context.Context, login SSHLoginDirect) (*auth.SSHLoginRes
 //
 // Returns the SSH certificate if authn is successful or an error.
 func SSHAgentPasswordlessLogin(ctx context.Context, login SSHLoginPasswordless) (*auth.SSHLoginResponse, error) {
-	webClient, webURL, err := initClient(login.ProxyAddr, login.Insecure, login.Pool)
+	webClient, webURL, err := initClient(login.ProxyAddr, login.Insecure, login.Pool, login.ExtraHeaders)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
@@ -466,7 +463,7 @@ func SSHAgentPasswordlessLogin(ctx context.Context, login SSHLoginPasswordless)
 // prompt the user to provide 2nd factor and pass the response to the proxy.
 // If the authentication succeeds, we will get a temporary certificate back.
 func SSHAgentMFALogin(ctx context.Context, login SSHLoginMFA) (*auth.SSHLoginResponse, error) {
-	clt, _, err := initClient(login.ProxyAddr, login.Insecure, login.Pool)
+	clt, _, err := initClient(login.ProxyAddr, login.Insecure, login.Pool, login.ExtraHeaders)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
@@ -534,7 +531,7 @@ func SSHAgentMFALogin(ctx context.Context, login SSHLoginMFA) (*auth.SSHLoginRes
 
 // HostCredentials is used to fetch host credentials for a node.
 func HostCredentials(ctx context.Context, proxyAddr string, insecure bool, req types.RegisterUsingTokenRequest) (*proto.Certs, error) {
-	clt, _, err := initClient(proxyAddr, insecure, nil)
+	clt, _, err := initClient(proxyAddr, insecure, nil, nil)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
@@ -554,7 +551,7 @@ func HostCredentials(ctx context.Context, proxyAddr string, insecure bool, req t
 
 // GetWebConfig is used by teleterm to fetch webconfig.js from proxies
 func GetWebConfig(ctx context.Context, proxyAddr string, insecure bool) (*webclient.WebConfig, error) {
-	clt, _, err := initClient(proxyAddr, insecure, nil)
+	clt, _, err := initClient(proxyAddr, insecure, nil, nil)
 	if err != nil {
 		return nil, trace.Wrap(err)
 	}
diff --git a/lib/client/weblogin_test.go b/lib/client/weblogin_test.go
index a562966a06e58..071ebcc69f022 100644
--- a/lib/client/weblogin_test.go
+++ b/lib/client/weblogin_test.go
@@ -36,69 +36,82 @@ import (
 	"github.com/gravitational/teleport/lib/client"
 )
 
-func TestPlainHttpFallback(t *testing.T) {
+// TestHostCredentialsHttpFallback tests that HostCredentials requests (/v1/webapi/host/credentials/)
+// fall back to HTTP only if the address is a loopback and the insecure mode was set.
+func TestHostCredentialsHttpFallback(t *testing.T) {
 	testCases := []struct {
-		desc            string
-		path            string
-		handler         http.HandlerFunc
-		actionUnderTest func(ctx context.Context, addr string, insecure bool) error
+		desc     string
+		loopback bool
+		insecure bool
+		fallback bool
 	}{
 		{
-			desc: "HostCredentials",
-			path: "/v1/webapi/host/credentials",
-			handler: func(w http.ResponseWriter, r *http.Request) {
-				if r.RequestURI != "/v1/webapi/host/credentials" {
-					w.WriteHeader(http.StatusNotFound)
-					return
-				}
-				w.Header().Set("Content-Type", "application/json")
-				w.WriteHeader(http.StatusOK)
-				json.NewEncoder(w).Encode(proto.Certs{})
-			},
-			actionUnderTest: func(ctx context.Context, addr string, insecure bool) error {
-				_, err := client.HostCredentials(ctx, addr, insecure, types.RegisterUsingTokenRequest{})
-				return err
-			},
+			desc:     "falls back to http if loopback and insecure",
+			loopback: true,
+			insecure: true,
+			fallback: true,
+		},
+		{
+			desc:     "does not fall back to http if loopback and secure",
+			loopback: true,
+			insecure: false,
+			fallback: false,
+		},
+		{
+			desc:     "does not fall back to http if non-loopback and insecure",
+			loopback: false,
+			insecure: true,
+			fallback: false,
 		},
 	}
 
-	for _, testCase := range testCases {
-		t.Run(testCase.desc, func(t *testing.T) {
-			ctx := context.Background()
-
-			t.Run("Allowed on insecure & loopback", func(t *testing.T) {
-				httpSvr := httptest.NewServer(testCase.handler)
-				defer httpSvr.Close()
-
-				err := testCase.actionUnderTest(ctx, httpSvr.Listener.Addr().String(), true /* insecure */)
-				require.NoError(t, err)
-			})
-
-			t.Run("Denied on secure", func(t *testing.T) {
-				httpSvr := httptest.NewServer(testCase.handler)
-				defer httpSvr.Close()
-
-				err := testCase.actionUnderTest(ctx, httpSvr.Listener.Addr().String(), false /* secure */)
-				require.Error(t, err)
-			})
+	for _, tc := range testCases {
+		// Start an http server (not https) so that the request only succeeds
+		// if the fallback occurs.
+		var handler http.HandlerFunc = func(w http.ResponseWriter, r *http.Request) {
+			if r.RequestURI != "/v1/webapi/host/credentials" {
+				w.WriteHeader(http.StatusNotFound)
+				return
+			}
+			w.Header().Set("Content-Type", "application/json")
+			w.WriteHeader(http.StatusOK)
+			json.NewEncoder(w).Encode(proto.Certs{})
+		}
+		httpSvr, err := newServer(handler, tc.loopback)
+		require.NoError(t, err)
+		defer httpSvr.Close()
+
+		// Send the HostCredentials request.
+		ctx := context.Background()
+		_, err = client.HostCredentials(ctx, httpSvr.Listener.Addr().String(), tc.insecure, types.RegisterUsingTokenRequest{})
+
+		// If it should fallback, then no error should occur
+		// as the request will hit the running http server.
+		if tc.fallback {
+			require.NoError(t, err)
+		} else {
+			require.Error(t, err)
+		}
+	}
+}
 
-			t.Run("Denied on non-loopback", func(t *testing.T) {
-				nonLoopbackSvr := httptest.NewUnstartedServer(testCase.handler)
+// newServer starts a new server that uses a loopback listener if `loopback`.
+func newServer(handler http.HandlerFunc, loopback bool) (*httptest.Server, error) {
+	srv := httptest.NewUnstartedServer(handler)
 
-				// replace the test-supplied loopback listener with the first available
-				// non-loopback address
-				nonLoopbackSvr.Listener.Close()
-				l, err := net.Listen("tcp", "0.0.0.0:0")
-				require.NoError(t, err)
-				nonLoopbackSvr.Listener = l
-				nonLoopbackSvr.Start()
-				defer nonLoopbackSvr.Close()
-
-				err = testCase.actionUnderTest(ctx, nonLoopbackSvr.Listener.Addr().String(), true /* insecure */)
-				require.Error(t, err)
-			})
-		})
+	if !loopback {
+		// Replace the test-supplied loopback listener with the first available
+		// non-loopback address.
+		srv.Listener.Close()
+		l, err := net.Listen("tcp", "0.0.0.0:0")
+		if err != nil {
+			return nil, err
+		}
+		srv.Listener = l
 	}
+
+	srv.Start()
+	return srv, nil
 }
 
 func TestSSHAgentPasswordlessLogin(t *testing.T) {