diff --git a/.ci/gen_certs.py b/.ci/gen_certs.py
new file mode 100644
index 000000000..e33e103ac
--- /dev/null
+++ b/.ci/gen_certs.py
@@ -0,0 +1,99 @@
+import argparse
+import os
+import sys
+from datetime import datetime
+from typing import List, Optional
+
+import trustme
+
+# ISO 8601
+DATE_FORMAT = "%Y-%m-%d"
+
+
+def main(argv: Optional[List[str]] = None) -> None:
+    if argv is None:
+        argv = sys.argv[1:]
+
+    parser = argparse.ArgumentParser(prog="trustme")
+    parser.add_argument(
+        "-d",
+        "--dir",
+        default=os.getcwd(),
+        help="Directory where certificates and keys are written to. Defaults to cwd.",
+    )
+    parser.add_argument(
+        "-i",
+        "--identities",
+        nargs="*",
+        default=("localhost", "127.0.0.1", "::1"),
+        help="Identities for the certificate. Defaults to 'localhost 127.0.0.1 ::1'.",
+    )
+    parser.add_argument(
+        "--common-name",
+        nargs=1,
+        default=None,
+        help="Also sets the deprecated 'commonName' field (only for the first identity passed).",
+    )
+    parser.add_argument(
+        "-x",
+        "--expires-on",
+        default=None,
+        help="Set the date the certificate will expire on (in YYYY-MM-DD format).",
+        metavar="YYYY-MM-DD",
+    )
+    parser.add_argument(
+        "-k",
+        "--key-type",
+        choices=list(t.name for t in trustme.KeyType),
+        default="ECDSA",
+    )
+
+    args = parser.parse_args(argv)
+    cert_dir = args.dir
+    identities = [str(identity) for identity in args.identities]
+    common_name = str(args.common_name[0]) if args.common_name else None
+    expires_on = (
+        None if args.expires_on is None else datetime.strptime(args.expires_on, DATE_FORMAT)
+    )
+    key_type = trustme.KeyType[args.key_type]
+
+    if not os.path.isdir(cert_dir):
+        raise ValueError(f"--dir={cert_dir} is not a directory")
+    if len(identities) < 1:
+        raise ValueError("Must include at least one identity")
+
+    # Generate the CA certificate
+    ca = trustme.CA(key_type=key_type)
+    # Write the certificate the client should trust
+    ca_cert_path = os.path.join(cert_dir, "ca.pem")
+    ca.cert_pem.write_to_path(path=ca_cert_path)
+
+    # Generate the server certificate
+    server_cert = ca.issue_cert(
+        *identities, common_name=common_name, not_after=expires_on, key_type=key_type
+    )
+    # Write the certificate and private key the server should use
+    server_key_path = os.path.join(cert_dir, "server.key")
+    server_cert_path = os.path.join(cert_dir, "server.pem")
+    server_cert.private_key_pem.write_to_path(path=server_key_path)
+    with open(server_cert_path, mode="w") as f:
+        f.truncate()
+    for blob in server_cert.cert_chain_pems:
+        blob.write_to_path(path=server_cert_path, append=True)
+
+    # Generate the client certificate
+    client_cert = ca.issue_cert(
+        "admin@example.com", common_name="admin", not_after=expires_on, key_type=key_type
+    )
+    # Write the certificate and private key the client should use
+    client_key_path = os.path.join(cert_dir, "client.key")
+    client_cert_path = os.path.join(cert_dir, "client.pem")
+    client_cert.private_key_pem.write_to_path(path=client_key_path)
+    with open(client_cert_path, mode="w") as f:
+        f.truncate()
+    for blob in client_cert.cert_chain_pems:
+        blob.write_to_path(path=client_cert_path, append=True)
+
+
+if __name__ == "__main__":
+    main()
diff --git a/.ci/nginx.conf.j2 b/.ci/nginx.conf.j2
new file mode 100644
index 000000000..70a2e5a3d
--- /dev/null
+++ b/.ci/nginx.conf.j2
@@ -0,0 +1,147 @@
+# Copy from pulp-oci-images.
+# Ideally we can get it upstream again.
+#
+# TODO: Support IPv6.
+# TODO: Maybe serve multiple `location`s, not just one.
+
+# The "nginx" package on fedora creates this user and group.
+user nginx nginx;
+# Gunicorn docs suggest this value.
+worker_processes 1;
+daemon off;
+events {
+    worker_connections 1024;  # increase if you have lots of clients
+    accept_mutex off;  # set to 'on' if nginx worker_processes > 1
+}
+
+http {
+    include mime.types;
+    # fallback in case we can't determine a type
+    default_type application/octet-stream;
+    sendfile on;
+
+    # If left at the default of 1024, nginx emits a warning about being unable
+    # to build optimal hash types.
+    types_hash_max_size 4096;
+
+    map $ssl_client_s_dn $ssl_client_s_dn_cn {
+        default "";
+        ~CN=(?<CN>[^,]+) $CN;
+    }
+
+    upstream pulp-content {
+         server 127.0.0.1:24816;
+    }
+
+    upstream pulp-api {
+         server 127.0.0.1:24817;
+    }
+
+    server {
+        # Gunicorn docs suggest the use of the "deferred" directive on Linux.
+        {% if https | default(false) -%}
+        listen 443 default_server deferred ssl;
+
+        ssl_certificate /etc/pulp/certs/pulp_webserver.crt;
+        ssl_certificate_key /etc/pulp/certs/pulp_webserver.key;
+        ssl_session_cache shared:SSL:50m;
+        ssl_session_timeout 1d;
+        ssl_session_tickets off;
+
+        # intermediate configuration
+        ssl_protocols TLSv1.2;
+        ssl_ciphers 'ECDHE-ECDSA-AES256-GCM-SHA384:ECDHE-RSA-AES256-GCM-SHA384:ECDHE-ECDSA-CHACHA20-POLY1305:ECDHE-RSA-CHACHA20-POLY1305:ECDHE-ECDSA-AES128-GCM-SHA256:ECDHE-RSA-AES128-GCM-SHA256:ECDHE-ECDSA-AES256-SHA384:ECDHE-RSA-AES256-SHA384:ECDHE-ECDSA-AES128-SHA256:ECDHE-RSA-AES128-SHA256';
+        ssl_prefer_server_ciphers on;
+
+        # HSTS (ngx_http_headers_module is required) (15768000 seconds = 6 months)
+        add_header Strict-Transport-Security max-age=15768000;
+
+        # Configure client cert authentication
+        ssl_client_certificate /etc/pulp/certs/ca.pem;
+        ssl_verify_client optional;
+        {%- else -%}
+        listen 80 default_server deferred;
+        {%- endif %}
+        server_name $hostname;
+
+        # The default client_max_body_size is 1m. Clients uploading
+        # files larger than this will need to chunk said files.
+        client_max_body_size 10m;
+
+        # Gunicorn docs suggest this value.
+        keepalive_timeout 5;
+
+        location {{ content_path }} {
+            proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
+            proxy_set_header X-Forwarded-Proto $scheme;
+            proxy_set_header Host $http_host;
+            # we don't want nginx trying to do something clever with
+            # redirects, we set the Host: header above already.
+            proxy_redirect off;
+            proxy_pass http://pulp-content;
+        }
+
+        location {{ api_root }}api/v3/ {
+            proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
+            proxy_set_header X-Forwarded-Proto $scheme;
+            proxy_set_header Host $http_host;
+            proxy_set_header Remoteuser $ssl_client_s_dn_cn;
+            # we don't want nginx trying to do something clever with
+            # redirects, we set the Host: header above already.
+            proxy_redirect off;
+            proxy_pass http://pulp-api;
+            client_max_body_size 0;
+        }
+
+        {%- if domain_enabled | default(false) %}
+        location ~ {{ api_root }}.+/api/v3/ {
+            proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
+            proxy_set_header X-Forwarded-Proto $scheme;
+            proxy_set_header Host $http_host;
+            # we don't want nginx trying to do something clever with
+            # redirects, we set the Host: header above already.
+            proxy_redirect off;
+            proxy_pass http://pulp-api;
+            client_max_body_size 0;
+        }
+        {%- endif %}
+
+        location /auth/login/ {
+            proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
+            proxy_set_header X-Forwarded-Proto $scheme;
+            proxy_set_header Host $http_host;
+            # we don't want nginx trying to do something clever with
+            # redirects, we set the Host: header above already.
+            proxy_redirect off;
+            proxy_pass http://pulp-api;
+        }
+
+        include pulp/*.conf;
+
+        location / {
+            proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
+            proxy_set_header X-Forwarded-Proto $scheme;
+            proxy_set_header Host $http_host;
+            # we don't want nginx trying to do something clever with
+            # redirects, we set the Host: header above already.
+            proxy_redirect off;
+            proxy_pass http://pulp-api;
+            # most pulp static files are served through whitenoise
+            # http://whitenoise.evans.io/en/stable/
+        }
+
+        {%- if https | default(false) %}
+        # ACME http-01 tokens, i.e, for Let's Encrypt
+        location /.well-known/ {
+            try_files $uri $uri/ =404;
+        }
+        {%- endif %}
+    }
+    {%- if https | default(false) %}
+    server {
+        listen 80 default_server;
+        server_name _;
+        return 301 https://$host$request_uri;
+    }
+    {%- endif %}
+}
diff --git a/.ci/run_container.sh b/.ci/run_container.sh
index 478b00b70..95084bd12 100755
--- a/.ci/run_container.sh
+++ b/.ci/run_container.sh
@@ -16,11 +16,12 @@ then
 fi
 export CONTAINER_RUNTIME
 
-TMPDIR="$(mktemp -d)"
+PULP_CLI_TEST_TMPDIR="$(mktemp -d)"
+export PULP_CLI_TEST_TMPDIR
 
 cleanup () {
   "${CONTAINER_RUNTIME}" stop pulp-ephemeral && true
-  rm -rf "${TMPDIR}"
+  rm -rf "${PULP_CLI_TEST_TMPDIR}"
 }
 
 trap cleanup EXIT
@@ -48,8 +49,8 @@ else
     SELINUX=""
 fi;
 
-mkdir -p "${TMPDIR}/settings/certs"
-cp "${BASEPATH}/settings/settings.py" "${TMPDIR}/settings"
+mkdir -p "${PULP_CLI_TEST_TMPDIR}/settings/certs"
+cp "${BASEPATH}/settings/settings.py" "${PULP_CLI_TEST_TMPDIR}/settings"
 
 if [ -z "${PULP_HTTPS:+x}" ]
 then
@@ -60,10 +61,16 @@ else
   PROTOCOL="https"
   PORT="443"
   PULP_CONTENT_ORIGIN="https://localhost:8080/"
-  python3 -m trustme -d "${TMPDIR}/settings/certs"
-  export PULP_CA_BUNDLE="${TMPDIR}/settings/certs/client.pem"
-  ln -fs server.pem "${TMPDIR}/settings/certs/pulp_webserver.crt"
-  ln -fs server.key "${TMPDIR}/settings/certs/pulp_webserver.key"
+  python3 "${BASEPATH}/gen_certs.py" -d "${PULP_CLI_TEST_TMPDIR}/settings/certs"
+  export PULP_CA_BUNDLE="${PULP_CLI_TEST_TMPDIR}/settings/certs/ca.pem"
+  ln -fs server.pem "${PULP_CLI_TEST_TMPDIR}/settings/certs/pulp_webserver.crt"
+  ln -fs server.key "${PULP_CLI_TEST_TMPDIR}/settings/certs/pulp_webserver.key"
+  {
+    echo "AUTHENTICATION_BACKENDS = '@json [\"django.contrib.auth.backends.RemoteUserBackend\"]'"
+    echo "MIDDLEWARE  = '@merge django.contrib.auth.middleware.RemoteUserMiddleware'"
+    echo "REST_FRAMEWORK__DEFAULT_AUTHENTICATION_CLASSES = '@merge pulpcore.app.authentication.PulpRemoteUserAuthentication'"
+    echo "REMOTE_USER_ENVIRON_NAME = 'HTTP_REMOTEUSER'"
+  } >> "${PULP_CLI_TEST_TMPDIR}/settings/settings.py"
 fi
 export PULP_CONTENT_ORIGIN
 
@@ -75,7 +82,8 @@ export PULP_CONTENT_ORIGIN
   --env PULP_CONTENT_ORIGIN \
   --detach \
   --name "pulp-ephemeral" \
-  --volume "${TMPDIR}/settings:/etc/pulp${SELINUX:+:Z}" \
+  --volume "${PULP_CLI_TEST_TMPDIR}/settings:/etc/pulp${SELINUX:+:Z}" \
+  --volume "${BASEPATH}/nginx.conf.j2:/nginx/nginx.conf.j2${SELINUX:+:Z}" \
   --network bridge \
   --publish "8080:${PORT}" \
   "ghcr.io/pulp/pulp:${IMAGE_TAG}"
@@ -105,7 +113,7 @@ done
 "${CONTAINER_RUNTIME}" exec "pulp-ephemeral" pulpcore-manager reset-admin-password --password password
 
 # Create pulp config
-PULP_CLI_CONFIG="${TMPDIR}/settings/certs/cli.toml"
+PULP_CLI_CONFIG="${PULP_CLI_TEST_TMPDIR}/settings/certs/cli.toml"
 export PULP_CLI_CONFIG
 pulp config create --overwrite --location "${PULP_CLI_CONFIG}" --base-url "${PROTOCOL}://localhost:8080" ${PULP_API_ROOT:+--api-root "${PULP_API_ROOT}"} --username "admin" --password "password"
 # show pulpcore/plugin versions we're using
diff --git a/pytest_pulp_cli/__init__.py b/pytest_pulp_cli/__init__.py
index 4b5aa743c..462240cf5 100644
--- a/pytest_pulp_cli/__init__.py
+++ b/pytest_pulp_cli/__init__.py
@@ -88,10 +88,16 @@ def pulp_cli_settings() -> t.Dict[str, t.Dict[str, t.Any]]:
     It is most likely not useful to be included standalone.
     The `pulp_cli_env` fixture, however depends on it and sets $XDG_CONFIG_HOME up accordingly.
     """
+    pulp_cli_test_tmpdir = pathlib.Path(os.environ.get("PULP_CLI_TEST_TMPDIR", "."))
     settings = toml.load(os.environ.get("PULP_CLI_CONFIG", "tests/cli.toml"))
     if os.environ.get("PULP_HTTPS"):
         for key in settings:
             settings[key]["base_url"] = settings[key]["base_url"].replace("http://", "https://")
+            settings[key].pop("username", None)
+            settings[key].pop("password", None)
+            settings[key]["cert"] = str(pulp_cli_test_tmpdir / "settings" / "certs" / "client.pem")
+            settings[key]["key"] = str(pulp_cli_test_tmpdir / "settings" / "certs" / "client.key")
+
     if os.environ.get("PULP_API_ROOT"):
         for key in settings:
             settings[key]["api_root"] = os.environ["PULP_API_ROOT"]