diff --git a/puppet/zulip/files/nginx/uwsgi_params b/puppet/zulip/files/nginx/uwsgi_params
index b18b74d026..09a1006932 100644
--- a/puppet/zulip/files/nginx/uwsgi_params
+++ b/puppet/zulip/files/nginx/uwsgi_params
@@ -16,5 +16,6 @@ uwsgi_param SERVER_NAME     $server_name;
 uwsgi_param HTTP_X_REAL_IP  $remote_addr;
 uwsgi_param HTTP_X_FORWARDED_PROTO $trusted_x_forwarded_proto;
 uwsgi_param HTTP_X_FORWARDED_SSL "";
+uwsgi_param HTTP_X_PROXY_MISCONFIGURATION $x_proxy_misconfiguration;
 
 uwsgi_pass django;
diff --git a/puppet/zulip/files/nginx/zulip-include-common/proxy b/puppet/zulip/files/nginx/zulip-include-common/proxy
index 4978da7fe8..e740420ccd 100644
--- a/puppet/zulip/files/nginx/zulip-include-common/proxy
+++ b/puppet/zulip/files/nginx/zulip-include-common/proxy
@@ -6,5 +6,6 @@ proxy_set_header Host $host;
 proxy_set_header X-Forwarded-Proto $trusted_x_forwarded_proto;
 proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
 proxy_set_header X-Real-Ip $remote_addr;
+proxy_set_header X-Proxy-Misconfiguration $x_proxy_misconfiguration;
 proxy_next_upstream off;
 proxy_redirect off;
diff --git a/puppet/zulip/templates/nginx/trusted-proto.template.erb b/puppet/zulip/templates/nginx/trusted-proto.template.erb
index 6a342fc840..ea764f367c 100644
--- a/puppet/zulip/templates/nginx/trusted-proto.template.erb
+++ b/puppet/zulip/templates/nginx/trusted-proto.template.erb
@@ -3,6 +3,10 @@
 map $remote_addr $trusted_x_forwarded_proto {
     default $scheme;
 }
+map $http_x_forwarded_for $x_proxy_misconfiguration {
+    default "";
+    "~." "No proxies configured in Zulip, but proxy headers detected from proxy at $remote_addr; see https://zulip.readthedocs.io/en/latest/production/deployment.html#putting-the-zulip-application-behind-a-reverse-proxy";
+}
 <% else %>
 # We do this in two steps because `geo` does not support variable
 # interpolation in the value, but does support CIDR notation,
@@ -18,4 +22,9 @@ map $is_x_forwarded_proto_trusted $trusted_x_forwarded_proto {
     0 $scheme;
     1 $http_x_forwarded_proto;
 }
+map "$is_x_forwarded_proto_trusted:$http_x_forwarded_proto" $x_proxy_misconfiguration {
+    "~^0:" "Incorrect reverse proxy IPs set in Zulip (try $remote_addr?); see https://zulip.readthedocs.io/en/latest/production/deployment.html#putting-the-zulip-application-behind-a-reverse-proxy";
+    "~^1:$" "No X-Forwarded-Proto header sent from trusted proxy $realip_remote_addr; see example configurations in https://zulip.readthedocs.io/en/latest/production/deployment.html#putting-the-zulip-application-behind-a-reverse-proxy";
+    default "";
+}
 <% end %>
diff --git a/zerver/middleware.py b/zerver/middleware.py
index 0d0c1a866d..30df1fcfb0 100644
--- a/zerver/middleware.py
+++ b/zerver/middleware.py
@@ -600,6 +600,50 @@ class SetRemoteAddrFromRealIpHeader(MiddlewareMixin):
             request.META["REMOTE_ADDR"] = real_ip
 
 
+class ProxyMisconfigurationError(JsonableError):
+    http_status_code = 500
+    data_fields = ["proxy_reason"]
+
+    def __init__(self, proxy_reason: str) -> None:
+        self.proxy_reason = proxy_reason
+
+    @staticmethod
+    def msg_format() -> str:
+        return _("Reverse proxy misconfiguration: {proxy_reason}")
+
+
+class DetectProxyMisconfiguration(MiddlewareMixin):
+    def process_view(
+        self,
+        request: HttpRequest,
+        view_func: Callable[Concatenate[HttpRequest, ParamT], HttpResponseBase],
+        args: List[object],
+        kwargs: Dict[str, Any],
+    ) -> None:
+        proxy_state_header = request.headers.get("X-Proxy-Misconfiguration", "")
+        # Our nginx configuration sets this header if:
+        #  - there is an X-Forwarded-For set but no proxies configured in Zulip
+        #  - proxies are configured but the request did not come from them
+        #  - proxies are configured and the request came from them,
+        #    but there was no X-Forwarded-Proto header
+        #
+        # Note that the first two may be false-positives.  We only
+        # display the error if the request also came in over HTTP (and
+        # a trusted proxy didn't say they get it over HTTPS), which
+        # should be impossible because Zulip only supports external
+        # https:// URLs in production.  nginx configuration ensures
+        # that request.is_secure() is only true if our nginx is
+        # serving the request over HTTPS, or it came from a trusted
+        # proxy which reports that it is doing so.  This will result
+        # in false negatives if Zulip's nginx is serving responses
+        # over HTTPS to a proxy whose IP is not configured, or
+        # misconfigured, but we cannot distinguish this from a random
+        # client which is providing proxy headers to a correctly
+        # configured Zulip.
+        if proxy_state_header != "" and not request.is_secure():
+            raise ProxyMisconfigurationError(proxy_state_header)
+
+
 def alter_content(request: HttpRequest, content: bytes) -> bytes:
     first_paragraph_text = get_content_description(content, request)
     placeholder_open_graph_description = RequestNotes.get_notes(
diff --git a/zproject/computed_settings.py b/zproject/computed_settings.py
index 9f2bcba168..8ffebe12d7 100644
--- a/zproject/computed_settings.py
+++ b/zproject/computed_settings.py
@@ -176,6 +176,7 @@ MIDDLEWARE = [
     "django.middleware.common.CommonMiddleware",
     "zerver.middleware.LocaleMiddleware",
     "zerver.middleware.HostDomainMiddleware",
+    "zerver.middleware.DetectProxyMisconfiguration",
     "django.middleware.csrf.CsrfViewMiddleware",
     # Make sure 2FA middlewares come after authentication middleware.
     "django_otp.middleware.OTPMiddleware",  # Required by two factor auth.