diff --git a/deploy/supervisor/deployment.yaml b/deploy/supervisor/deployment.yaml
index 1e0c75c0a..effba2fb7 100644
--- a/deploy/supervisor/deployment.yaml
+++ b/deploy/supervisor/deployment.yaml
@@ -1,4 +1,4 @@
-#! Copyright 2020 the Pinniped contributors. All Rights Reserved.
+#! Copyright 2020-2021 the Pinniped contributors. All Rights Reserved.
 #! SPDX-License-Identifier: Apache-2.0
 
 #@ load("@ytt:data", "data")
@@ -101,6 +101,15 @@ spec:
               protocol: TCP
             - containerPort: 8443
               protocol: TCP
+          env:
+            #@ if data.values.https_proxy:
+            - name: HTTPS_PROXY
+              value: #@ data.values.https_proxy
+            #@ end
+            #@ if data.values.no_proxy:
+            - name: NO_PROXY
+              value: #@ data.values.no_proxy
+            #@ end
           livenessProbe:
             httpGet:
               path: /healthz
diff --git a/deploy/supervisor/values.yaml b/deploy/supervisor/values.yaml
index a4575c3c6..62b632f7d 100644
--- a/deploy/supervisor/values.yaml
+++ b/deploy/supervisor/values.yaml
@@ -1,4 +1,4 @@
-#! Copyright 2020 the Pinniped contributors. All Rights Reserved.
+#! Copyright 2020-2021 the Pinniped contributors. All Rights Reserved.
 #! SPDX-License-Identifier: Apache-2.0
 
 #@data/values
@@ -56,3 +56,11 @@ service_loadbalancer_ip: #! e.g. 1.2.3.4
 #! Specify the verbosity of logging: info ("nice to know" information), debug (developer
 #! information), trace (timing information), all (kitchen sink).
 log_level: #! By default, when this value is left unset, only warnings and errors are printed. There is no way to suppress warning and error logs.
+
+#! Set the standard golang HTTPS_PROXY and NO_PROXY environment variables on the Supervisor containers.
+#! These will be used when the Supervisor makes backend-to-backend calls to upstream identity providers using HTTPS,
+#! e.g. when the Supervisor fetches discovery documents, JWKS keys, and tokens from an upstream OIDC Provider.
+#! The Supervisor never makes insecure HTTP calls, so there is no reason to set HTTP_PROXY.
+#! Optional.
+https_proxy: #! e.g. http://proxy.example.com
+no_proxy: #! e.g. 127.0.0.1
diff --git a/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher.go b/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher.go
index b6b553283..edf9ba387 100644
--- a/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher.go
+++ b/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher.go
@@ -265,9 +265,13 @@ func (c *controller) validateIssuer(ctx context.Context, upstream *v1alpha1.OIDC
 				Message: err.Error(),
 			}
 		}
-		httpClient = &http.Client{Transport: &http.Transport{TLSClientConfig: tlsConfig}}
 
-		discoveredProvider, err = oidc.NewProvider(oidc.ClientContext(ctx, httpClient), upstream.Spec.Issuer)
+		httpClient = &http.Client{Transport: &http.Transport{Proxy: http.ProxyFromEnvironment, TLSClientConfig: tlsConfig}}
+
+		timeoutCtx, cancelFunc := context.WithTimeout(oidc.ClientContext(ctx, httpClient), time.Minute)
+		defer cancelFunc()
+
+		discoveredProvider, err = oidc.NewProvider(timeoutCtx, upstream.Spec.Issuer)
 		if err != nil {
 			return &v1alpha1.Condition{
 				Type:    typeOIDCDiscoverySucceeded,
diff --git a/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher_test.go b/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher_test.go
index 02e96e8ee..4b97a07be 100644
--- a/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher_test.go
+++ b/internal/controller/supervisorconfig/upstreamwatcher/upstreamwatcher_test.go
@@ -9,6 +9,7 @@ import (
 	"encoding/json"
 	"net/http"
 	"net/url"
+	"reflect"
 	"strings"
 	"testing"
 	"time"
@@ -650,6 +651,15 @@ func TestController(t *testing.T) {
 				require.Equal(t, tt.wantResultingCache[i].GetUsernameClaim(), actualIDP.GetUsernameClaim())
 				require.Equal(t, tt.wantResultingCache[i].GetGroupsClaim(), actualIDP.GetGroupsClaim())
 				require.ElementsMatch(t, tt.wantResultingCache[i].GetScopes(), actualIDP.GetScopes())
+
+				// We always want to use the proxy from env on these clients, so although the following assertions
+				// are a little hacky, this is a cheap way to test that we are using it.
+				actualTransport, ok := actualIDP.Client.Transport.(*http.Transport)
+				require.True(t, ok, "expected cached provider to have client with Transport of type *http.Transport")
+				httpProxyFromEnvFunction := reflect.ValueOf(http.ProxyFromEnvironment).Pointer()
+				actualTransportProxyFunction := reflect.ValueOf(actualTransport.Proxy).Pointer()
+				require.Equal(t, httpProxyFromEnvFunction, actualTransportProxyFunction,
+					"Transport should have used http.ProxyFromEnvironment as its Proxy func")
 			}
 
 			actualUpstreams, err := fakePinnipedClient.IDPV1alpha1().OIDCIdentityProviders(testNamespace).List(ctx, metav1.ListOptions{})