diff --git a/.github/workflows/no_zombies.yml b/.github/workflows/no_zombies.yml
index 83f8a560dfd..b0d9a5379cc 100644
--- a/.github/workflows/no_zombies.yml
+++ b/.github/workflows/no_zombies.yml
@@ -42,5 +42,5 @@ jobs:
         pip install .
 
         # ensure kolibri stops within 20 seconds 10 times in a row
-        ./test/ensure_kolibri_stops_within_time.sh 20 10 8082
+        ./test/ensure_kolibri_stops_within_time.sh 20 10 8082 8083
         ./test/ensure_no_kolibris_running_on_port.sh 8082
diff --git a/kolibri/core/content/utils/paths.py b/kolibri/core/content/utils/paths.py
index 794fdf8f28c..bfab772eeee 100644
--- a/kolibri/core/content/utils/paths.py
+++ b/kolibri/core/content/utils/paths.py
@@ -8,6 +8,7 @@
 
 from kolibri.core.content.errors import InvalidStorageFilenameError
 from kolibri.utils import conf
+from kolibri.utils.server import get_zip_port
 
 
 # valid storage filenames consist of 32-char hex plus a file extension
@@ -253,6 +254,20 @@ def get_file_checksums_url(channel_id, baseurl, version="1"):
 ZIPCONTENT = "zipcontent/"
 
 
+def get_zip_content_config():
+    zip_content_origin = conf.OPTIONS["Deployment"]["ZIP_CONTENT_ORIGIN"]
+    if not zip_content_origin:
+        zip_content_port = str(
+            get_zip_port() or conf.OPTIONS["Deployment"]["ZIP_CONTENT_PORT"]
+        )
+    elif type(zip_content_origin) is int:
+        zip_content_port = str(zip_content_origin)
+        zip_content_origin = ""
+    else:
+        zip_content_port = ""
+    return zip_content_origin, zip_content_port
+
+
 def zip_content_path_prefix():
     path_prefix = conf.OPTIONS["Deployment"]["ZIP_CONTENT_URL_PATH_PREFIX"]
 
diff --git a/kolibri/core/kolibri_plugin.py b/kolibri/core/kolibri_plugin.py
index 8786fd5ba0e..bb8080df1f3 100644
--- a/kolibri/core/kolibri_plugin.py
+++ b/kolibri/core/kolibri_plugin.py
@@ -19,6 +19,7 @@
 from kolibri.core.content.utils.paths import get_content_storage_url
 from kolibri.core.content.utils.paths import get_hashi_path
 from kolibri.core.content.utils.paths import get_zip_content_base_path
+from kolibri.core.content.utils.paths import get_zip_content_config
 from kolibri.core.device.models import ContentCacheKey
 from kolibri.core.device.utils import allow_other_browsers_to_connect
 from kolibri.core.hooks import NavigationHook
@@ -53,14 +54,7 @@ def url_tag(self):
             # For some reason the js_name gets escaped going into the template
             # so this was the easiest way to inject it.
         ).replace("__placeholder__", js_name)
-        zip_content_origin = OPTIONS["Deployment"]["ZIP_CONTENT_ORIGIN"]
-        if not zip_content_origin:
-            zip_content_port = str(OPTIONS["Deployment"]["ZIP_CONTENT_PORT"])
-        elif type(zip_content_origin) is int:
-            zip_content_port = str(zip_content_origin)
-            zip_content_origin = ""
-        else:
-            zip_content_port = ""
+        zip_content_origin, zip_content_port = get_zip_content_config()
         return [
             mark_safe(
                 """<script type="text/javascript">"""
diff --git a/kolibri/utils/cli.py b/kolibri/utils/cli.py
index 1ce45a0216c..79fc56d9bc4 100644
--- a/kolibri/utils/cli.py
+++ b/kolibri/utils/cli.py
@@ -454,17 +454,26 @@ def main(ctx):
     type=int,
     help="Port on which Kolibri is being served",
 )
+@click.option(
+    "--zip-port",
+    default=OPTIONS["Deployment"]["ZIP_CONTENT_PORT"],
+    type=int,
+    help="Port on which zip content server is being served",
+)
 @click.option(
     "--background/--foreground",
     default=True,
     help="Run Kolibri as a background process",
 )
-def start(port, background):
+def start(port, zip_port, background):
     """
     Start the server on given port.
     """
     server.start(
-        port=port, serve_http=OPTIONS["Server"]["CHERRYPY_START"], background=background
+        port=port,
+        zip_port=zip_port,
+        serve_http=OPTIONS["Server"]["CHERRYPY_START"],
+        background=background,
     )
 
 
@@ -530,7 +539,7 @@ def status():
     "--port",
     default=OPTIONS["Deployment"]["HTTP_PORT"],
     type=int,
-    help="Port on which to run Kolibri services",
+    help="Port on which Kolibri is running to inform services",
 )
 @click.option(
     "--background/--foreground",
@@ -544,7 +553,7 @@ def services(port, background):
 
     logger.info("Starting Kolibri background services")
 
-    server.start(port=port, serve_http=False, background=background)
+    server.start(port=port, zip_port=None, serve_http=False, background=background)
 
 
 def setup_logging(debug=False, debug_database=False):
diff --git a/kolibri/utils/options.py b/kolibri/utils/options.py
index c4b797a4182..9766c6b21db 100644
--- a/kolibri/utils/options.py
+++ b/kolibri/utils/options.py
@@ -208,7 +208,7 @@ def path_list(value):
 
 
 def validate_port_number(value):
-    if 1 <= value <= 65535:
+    if 0 <= value <= 65535:
         return value
     raise VdtValueError(value)
 
@@ -418,7 +418,7 @@ def origin_or_port(value):
         },
         "ZIP_CONTENT_PORT": {
             "type": "port",
-            "default": 8765,
+            "default": 0,
             "envvars": ("KOLIBRI_ZIP_CONTENT_PORT",),
         },
         "ZIP_CONTENT_URL_PATH_PREFIX": {
diff --git a/kolibri/utils/server.py b/kolibri/utils/server.py
index 2893210ced0..573ee50c0c8 100644
--- a/kolibri/utils/server.py
+++ b/kolibri/utils/server.py
@@ -206,13 +206,15 @@ def STOP(self):
 
 
 class PIDPlugin(SimplePlugin):
-    def __init__(self, bus, port, pid_file=PID_FILE):
+    def __init__(self, bus, port, zip_port, pid_file=PID_FILE):
         self.bus = bus
         self.port = port
+        self.zip_port = zip_port
         self.pid_file = pid_file
         # Do this during initialization to set a startup lock
         self.set_pid_file(STATUS_STARTING_UP)
         self.bus.subscribe("SERVING", self.SERVING)
+        self.bus.subscribe("ZIP_SERVING", self.ZIP_SERVING)
         for bus_status, status in status_map.items():
             handler = partial(self.set_pid_file, status)
             handler.priority = 10
@@ -225,10 +227,17 @@ def set_pid_file(self, status):
         :param: status: status of the process
         """
         with open(self.pid_file, "w") as f:
-            f.write("{}\n{}\n{}\n".format(os.getpid(), self.port, status))
+            f.write(
+                "{}\n{}\n{}\n{}\n".format(os.getpid(), self.port, self.zip_port, status)
+            )
 
     def SERVING(self, port):
         self.port = port or self.port
+        self.set_pid_file(STATUS_RUNNING)
+
+    def ZIP_SERVING(self, zip_port):
+        self.zip_port = zip_port or self.zip_port
+        self.set_pid_file(STATUS_RUNNING)
 
     def EXIT(self):
         try:
@@ -304,7 +313,7 @@ def stop():
     Stops the kolibri server
     :raises: NotRunning
     """
-    pid, __, status = _read_pid_file(PID_FILE)
+    pid, __, __, status = _read_pid_file(PID_FILE)
 
     if not pid:
         return status
@@ -335,7 +344,7 @@ def stop():
     return STATUS_STOPPED
 
 
-def configure_http_server(port, bus):
+def configure_http_server(port, zip_port, bus):
     from kolibri.deployment.default.wsgi import application
     from kolibri.deployment.default.alt_wsgi import alt_application
 
@@ -357,7 +366,7 @@ def configure_http_server(port, bus):
 
     alt_port_addr = (
         LISTEN_ADDRESS,
-        conf.OPTIONS["Deployment"]["ZIP_CONTENT_PORT"],
+        zip_port,
     )
 
     alt_port_server = ServerPlugin(
@@ -390,11 +399,11 @@ def check_port_availability(host, port):
             sys.exit(1)
 
 
-def start(port=8080, serve_http=True, background=False):
+def start(port=0, zip_port=0, serve_http=True, background=False):
     """
     Starts the server.
 
-    :param: port: Port number (default: 8080)
+    :param: port: Port number (default: 0) - assigned by free port
     """
     # On Mac, Python crashes when forking the process, so prevent daemonization until we can figure out
     # a better fix. See https://github.com/learningequality/kolibri/issues/4821
@@ -403,7 +412,7 @@ def start(port=8080, serve_http=True, background=False):
 
     # Check if there are other kolibri instances running
     # If there are, then we need to stop users from starting kolibri again.
-    pid, port, status = _read_pid_file(PID_FILE)
+    _, _, _, status = _read_pid_file(PID_FILE)
 
     if status in IS_RUNNING:
         logger.error(
@@ -417,7 +426,7 @@ def start(port=8080, serve_http=True, background=False):
     # Setup plugin for handling PID file cleanup
     # Do this first to obtain a PID file lock as soon as
     # possible and reduce the risk of competing servers
-    pid_plugin = PIDPlugin(bus, port)
+    pid_plugin = PIDPlugin(bus, port, zip_port)
     pid_plugin.subscribe()
 
     if background and serve_http:
@@ -444,7 +453,7 @@ def start(port=8080, serve_http=True, background=False):
     log_plugin.subscribe()
 
     if serve_http:
-        configure_http_server(port, bus)
+        configure_http_server(port, zip_port, bus)
 
     # Setup plugin for services
     service_plugin = ServicesPlugin(bus, port)
@@ -478,18 +487,24 @@ def _read_pid_file(filename):
                           port is None.
     """
     if not os.path.isfile(PID_FILE):
-        return None, None, STATUS_STOPPED
+        return None, None, None, STATUS_STOPPED
 
     try:
         pid_file_lines = open(filename, "r").readlines()
-        pid, port, status = pid_file_lines
+        pid, port, zip_port, status = pid_file_lines
         pid = int(pid.strip())
         port = int(port.strip()) if port.strip() else None
+        zip_port = int(zip_port.strip()) if zip_port.strip() else None
         status = int(status.strip())
-        return pid, port, status
+        return pid, port, zip_port, status
     except (TypeError, ValueError, IOError, OSError):
         pass
-    return None, None, STATUS_PID_FILE_INVALID
+    return None, None, None, STATUS_PID_FILE_INVALID
+
+
+def get_zip_port():
+    _, _, zip_port, _ = _read_pid_file(PID_FILE)
+    return zip_port
 
 
 def get_status():  # noqa: max-complexity=16
@@ -506,7 +521,7 @@ def get_status():  # noqa: max-complexity=16
     :raises: NotRunning
     """
     # PID file exists and startup has finished, check if it is running
-    pid, port, status = _read_pid_file(PID_FILE)
+    pid, port, _, status = _read_pid_file(PID_FILE)
 
     if status not in IS_RUNNING:
         raise NotRunning(status)
diff --git a/test/ensure_kolibri_stops_within_time.sh b/test/ensure_kolibri_stops_within_time.sh
index 4a318ffe36d..ea66cb484b4 100755
--- a/test/ensure_kolibri_stops_within_time.sh
+++ b/test/ensure_kolibri_stops_within_time.sh
@@ -3,7 +3,7 @@
 MAX=0
 for i in $(seq 1 $2)
 do
-  kolibri start --port=$3 > /dev/null 2>&1
+  kolibri start --port=$3 --zip-port=$4 > /dev/null 2>&1
   START_TIME=$SECONDS
   kolibri stop > /dev/null 2>&1
   ELAPSED_TIME=$(($SECONDS - $START_TIME))