--- a/testing/web-platform/tests/tools/wptrunner/tox.ini
+++ b/testing/web-platform/tests/tools/wptrunner/tox.ini
@@ -1,13 +1,13 @@
 [pytest]
 xfail_strict=true
 
 [tox]
-envlist = py27-{base,chrome,edge,firefox,ie,opera,safari,sauce,servo},py36-base
+envlist = py27-{base,chrome,edge,firefox,ie,opera,safari,sauce,servo,webkit,webkitgtk_minibrowser,epiphany},py36-base
 skip_missing_interpreters = true
 
 [testenv]
 deps =
      pytest>=2.9
      pytest-cov
      pytest-xdist
      mock
@@ -15,15 +15,18 @@ deps =
      chrome: -r{toxinidir}/requirements_chrome.txt
      edge: -r{toxinidir}/requirements_edge.txt
      firefox: -r{toxinidir}/requirements_firefox.txt
      ie: -r{toxinidir}/requirements_ie.txt
      opera: -r{toxinidir}/requirements_opera.txt
      safari: -r{toxinidir}/requirements_safari.txt
      sauce: -r{toxinidir}/requirements_sauce.txt
      servo: -r{toxinidir}/requirements_servo.txt
+     webkit: -r{toxinidir}/requirements_webkit.txt
+     webkitgtk_minibrowser: -r{toxinidir}/requirements_webkit.txt
+     epiphany: -r{toxinidir}/requirements_epiphany.txt
 
 commands = pytest {posargs}
 
 setenv = CURRENT_TOX_ENV = {envname}
 
 passenv =
   TASKCLUSTER_ROOT_URL

--- a/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/base.py
+++ b/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/base.py
@@ -69,16 +69,24 @@ def maybe_add_args(required_args, curren
             if not any(item.startswith(required_arg_prefix) for item in current_args):
                 current_args.append(required_arg)
         else:
             if required_arg not in current_args:
                 current_args.append(required_arg)
     return current_args
 
 
+def certificate_domain_list(list_of_domains, certificate_file):
+    """Build a list of domains where certificate_file should be used"""
+    cert_list = []
+    for domain in list_of_domains:
+        cert_list.append({"host": domain, "certificateFile": certificate_file})
+    return cert_list
+
+
 def get_free_port():
     """Get a random unbound port"""
     while True:
         s = socket.socket()
         try:
             s.bind(("127.0.0.1", 0))
         except socket.error:
             continue

--- a/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/epiphany.py
+++ b/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/epiphany.py
@@ -1,9 +1,9 @@
-from .base import get_timeout_multiplier, maybe_add_args   # noqa: F401
+from .base import get_timeout_multiplier, maybe_add_args, certificate_domain_list  # noqa: F401
 from .webkit import WebKitBrowser
 from ..executors import executor_kwargs as base_executor_kwargs
 from ..executors.executorwebdriver import (WebDriverTestharnessExecutor,  # noqa: F401
                                            WebDriverRefTestExecutor)  # noqa: F401
 from ..executors.executorwebkit import WebKitDriverWdspecExecutor  # noqa: F401
 
 __wptrunner__ = {"product": "epiphany",
                  "check_args": "check_args",
@@ -39,19 +39,17 @@ def capabilities(server_config, **kwargs
 
     return {
         "browserName": "Epiphany",
         "browserVersion": "3.31.4",  # First version to support automation
         "platformName": "ANY",
         "webkitgtk:browserOptions": {
             "binary": kwargs["binary"],
             "args": args,
-            "certificates": [
-                {"host": server_config["browser_host"],
-                 "certificateFile": kwargs["host_cert_path"]}]}}
+            "certificates": certificate_domain_list(server_config.domains_set, kwargs["host_cert_path"])}}
 
 
 def executor_kwargs(test_type, server_config, cache_manager, run_info_data,
                     **kwargs):
     executor_kwargs = base_executor_kwargs(test_type, server_config,
                                            cache_manager, run_info_data, **kwargs)
     executor_kwargs["close_after_done"] = True
     executor_kwargs["capabilities"] = capabilities(server_config, **kwargs)

--- a/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/webkit.py
+++ b/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/webkit.py
@@ -1,10 +1,10 @@
 from .base import Browser, ExecutorBrowser, require_arg
-from .base import get_timeout_multiplier   # noqa: F401
+from .base import get_timeout_multiplier, certificate_domain_list  # noqa: F401
 from ..executors import executor_kwargs as base_executor_kwargs
 from ..executors.executorwebdriver import (WebDriverTestharnessExecutor,  # noqa: F401
                                            WebDriverRefTestExecutor)  # noqa: F401
 from ..executors.executorwebkit import WebKitDriverWdspecExecutor  # noqa: F401
 from ..webdriver_server import WebKitDriverServer
 
 
 __wptrunner__ = {"product": "webkit",
@@ -42,19 +42,17 @@ def capabilities_for_port(server_config,
 
         return {
             "browserName": "MiniBrowser",
             "browserVersion": "2.20",
             "platformName": "ANY",
             browser_options_key: {
                 "binary": kwargs["binary"],
                 "args": kwargs.get("binary_args", []),
-                "certificates": [
-                    {"host": server_config["browser_host"],
-                     "certificateFile": kwargs["host_cert_path"]}]}}
+                "certificates": certificate_domain_list(server_config.domains_set, kwargs["host_cert_path"])}}
 
     return {}
 
 
 def executor_kwargs(test_type, server_config, cache_manager, run_info_data,
                     **kwargs):
     executor_kwargs = base_executor_kwargs(test_type, server_config,
                                            cache_manager, run_info_data, **kwargs)

--- a/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/webkitgtk_minibrowser.py
+++ b/testing/web-platform/tests/tools/wptrunner/wptrunner/browsers/webkitgtk_minibrowser.py
@@ -1,9 +1,9 @@
-from .base import get_timeout_multiplier, maybe_add_args   # noqa: F401
+from .base import get_timeout_multiplier, maybe_add_args, certificate_domain_list  # noqa: F401
 from .webkit import WebKitBrowser
 from ..executors import executor_kwargs as base_executor_kwargs
 from ..executors.executorwebdriver import (WebDriverTestharnessExecutor,  # noqa: F401
                                            WebDriverRefTestExecutor)  # noqa: F401
 from ..executors.executorwebkit import WebKitDriverWdspecExecutor  # noqa: F401
 
 __wptrunner__ = {"product": "webkitgtk_minibrowser",
                  "check_args": "check_args",
@@ -43,19 +43,17 @@ def capabilities(server_config, **kwargs
                             "--enable-webaudio=true"]
     args = kwargs.get("binary_args", [])
     args = maybe_add_args(browser_required_args, args)
     return {
         "browserName": "MiniBrowser",
         "webkitgtk:browserOptions": {
             "binary": kwargs["binary"],
             "args": args,
-            "certificates": [
-                {"host": server_config["browser_host"],
-                 "certificateFile": kwargs["host_cert_path"]}]}}
+            "certificates": certificate_domain_list(server_config.domains_set, kwargs["host_cert_path"])}}
 
 
 def executor_kwargs(test_type, server_config, cache_manager, run_info_data,
                     **kwargs):
     executor_kwargs = base_executor_kwargs(test_type, server_config,
                                            cache_manager, run_info_data, **kwargs)
     executor_kwargs["close_after_done"] = True
     executor_kwargs["capabilities"] = capabilities(server_config, **kwargs)

new file mode 100644
--- /dev/null
+++ b/testing/web-platform/tests/tools/wptrunner/wptrunner/tests/browsers/test_webkitgtk.py
@@ -0,0 +1,57 @@
+from os.path import join, dirname
+
+import pytest
+
+from wptserve.config import ConfigBuilder
+from ..base import active_products
+from wptrunner import environment, products
+
+test_paths = {"/": {"tests_path": join(dirname(__file__), "..", "..", "..", "..", "..")}}  # repo root
+environment.do_delayed_imports(None, test_paths)
+
+
+@active_products("product")
+def test_webkitgtk_certificate_domain_list(product):
+
+    def domain_is_inside_certificate_list_cert(domain_to_find, webkitgtk_certificate_list, cert_file):
+        for domain in webkitgtk_certificate_list:
+            if domain["host"] == domain_to_find and domain["certificateFile"] == cert_file:
+                return True
+        return False
+
+    if product not in ["epiphany", "webkit", "webkitgtk_minibrowser"]:
+        pytest.skip("%s doesn't support certificate_domain_list" % product)
+
+    (check_args,
+     target_browser_cls, get_browser_kwargs,
+     executor_classes, get_executor_kwargs,
+     env_options, get_env_extras, run_info_extras) = products.load_product({}, product)
+
+    cert_file = "/home/user/wpt/tools/certs/cacert.pem"
+    valid_domains_test = ["a.example.org", "b.example.org", "example.org",
+                          "a.example.net", "b.example.net", "example.net"]
+    invalid_domains_test = ["x.example.org", "y.example.org", "example.it",
+                            "x.example.net", "y.example.net", "z.example.net"]
+    kwargs = {}
+    kwargs["timeout_multiplier"] = 1
+    kwargs["debug_info"] = None
+    kwargs["host_cert_path"] = cert_file
+    kwargs["webkit_port"] = "gtk"
+    kwargs["binary"] = None
+    kwargs["webdriver_binary"] = None
+    with ConfigBuilder(browser_host="example.net",
+                       alternate_hosts={"alt": "example.org"},
+                       subdomains={"a", "b"},
+                       not_subdomains={"x", "y"}) as env_config:
+
+        executor_args = get_executor_kwargs(None, env_config, None, None, **kwargs)
+        assert('capabilities' in executor_args)
+        assert('webkitgtk:browserOptions' in executor_args['capabilities'])
+        assert('certificates' in executor_args['capabilities']['webkitgtk:browserOptions'])
+        cert_list = executor_args['capabilities']['webkitgtk:browserOptions']['certificates']
+        for valid_domain in valid_domains_test:
+            assert(domain_is_inside_certificate_list_cert(valid_domain, cert_list, cert_file))
+            assert(not domain_is_inside_certificate_list_cert(valid_domain, cert_list, cert_file + ".backup_non_existent"))
+        for invalid_domain in invalid_domains_test:
+            assert(not domain_is_inside_certificate_list_cert(invalid_domain, cert_list, cert_file))
+            assert(not domain_is_inside_certificate_list_cert(invalid_domain, cert_list, cert_file + ".backup_non_existent"))