diff --git a/py/BUILD.bazel b/py/BUILD.bazel
index 7cddd0d8515b8..530fd4d8d19f7 100644
--- a/py/BUILD.bazel
+++ b/py/BUILD.bazel
@@ -321,7 +321,6 @@ py_library(
         "test/selenium/webdriver/__init__.py",
         "test/selenium/webdriver/chrome/__init__.py",
         "test/selenium/webdriver/common/__init__.py",
-        "test/selenium/webdriver/common/conftest.py",
         "test/selenium/webdriver/common/network.py",
         "test/selenium/webdriver/common/webserver.py",
         "test/selenium/webdriver/firefox/__init__.py",
@@ -330,7 +329,6 @@ py_library(
         "test/selenium/webdriver/marionette/conftest.py",
         "test/selenium/webdriver/safari/conftest.py",
         "test/selenium/webdriver/support/__init__.py",
-        "test/selenium/webdriver/support/conftest.py",
     ],
     data = [
         "pyproject.toml",
@@ -547,6 +545,7 @@ py_test_suite(
     srcs = glob(
         [
             "test/selenium/webdriver/common/**/*.py",
+            "test/selenium/webdriver/remote/**/*.py",
             "test/selenium/webdriver/support/**/*.py",
         ],
         exclude = BIDI_TESTS,
diff --git a/py/conftest.py b/py/conftest.py
index 71d7103bbb045..b076e18313e71 100644
--- a/py/conftest.py
+++ b/py/conftest.py
@@ -96,6 +96,11 @@ def pytest_ignore_collect(path, config):
     return len([d for d in _drivers if d.lower() in parts]) > 0
 
 
+def pytest_generate_tests(metafunc):
+    if "driver" in metafunc.fixturenames and metafunc.config.option.drivers:
+        metafunc.parametrize("driver", metafunc.config.option.drivers, indirect=True)
+
+
 def get_driver_class(driver_option):
     """Generate the driver class name from the lowercase driver option."""
     if driver_option == "webkitgtk":
@@ -113,9 +118,16 @@ def get_driver_class(driver_option):
 @pytest.fixture(scope="function")
 def driver(request):
     kwargs = {}
+    driver_option = getattr(request, "param", "Chrome")
+
     # browser can be changed with `--driver=firefox` as an argument or to addopts in pytest.ini
-    driver_class = get_driver_class(getattr(request, "param", "Chrome"))
-    # skip tests if not available on the platform
+    driver_class = get_driver_class(driver_option)
+
+    # skip tests in the 'remote' directory if run with a local driver
+    if request.node.path.parts[-2] == "remote" and driver_class != "Remote":
+        pytest.skip(f"Remote tests can't be run with driver '{driver_option}'")
+
+    # skip tests that can't run on certain platforms
     _platform = platform.system()
     if driver_class == "Safari" and _platform != "Darwin":
         pytest.skip("Safari tests can only run on an Apple OS")
@@ -123,10 +135,12 @@ def driver(request):
         pytest.skip("IE and EdgeHTML Tests can only run on Windows")
     if "WebKit" in driver_class and _platform == "Windows":
         pytest.skip("WebKit tests cannot be run on Windows")
+
     # skip tests for drivers that don't support BiDi when --bidi is enabled
     if request.config.option.bidi:
         if driver_class in ("Ie", "Safari", "WebKitGTK", "WPEWebKit"):
             pytest.skip(f"{driver_class} does not support BiDi")
+
     # conditionally mark tests as expected to fail based on driver
     marker = request.node.get_closest_marker(f"xfail_{driver_class.lower()}")
 
@@ -177,6 +191,7 @@ def fin():
             kwargs["options"] = options
 
         driver_instance = getattr(webdriver, driver_class)(**kwargs)
+
     yield driver_instance
     # Close the browser after BiDi tests. Those make event subscriptions
     # and doesn't seems to be stable enough, causing the flakiness of the
@@ -217,7 +232,6 @@ def get_options(driver_class, config):
     if headless:
         if not options:
             options = getattr(webdriver, f"{driver_class}Options")()
-
         if driver_class == "Chrome" or driver_class == "Edge":
             options.add_argument("--headless=new")
         if driver_class == "Firefox":
@@ -226,7 +240,6 @@ def get_options(driver_class, config):
     if bidi:
         if not options:
             options = getattr(webdriver, f"{driver_class}Options")()
-
         options.web_socket_url = True
         options.unhandled_prompt_behavior = "ignore"
 
@@ -382,3 +395,11 @@ def clean_driver(request):
 
     if request.node.get_closest_marker("no_driver_after_test"):
         driver_reference = None
+
+
+@pytest.fixture
+def firefox_options(request):
+    options = webdriver.FirefoxOptions()
+    if request.config.option.headless:
+        options.add_argument("-headless")
+    return options
diff --git a/py/test/selenium/webdriver/chrome/conftest.py b/py/test/selenium/webdriver/chrome/conftest.py
deleted file mode 100644
index 043b7df7e146f..0000000000000
--- a/py/test/selenium/webdriver/chrome/conftest.py
+++ /dev/null
@@ -1,21 +0,0 @@
-# Licensed to the Software Freedom Conservancy (SFC) under one
-# or more contributor license agreements.  See the NOTICE file
-# distributed with this work for additional information
-# regarding copyright ownership.  The SFC licenses this file
-# to you under the Apache License, Version 2.0 (the
-# "License"); you may not use this file except in compliance
-# with the License.  You may obtain a copy of the License at
-#
-#   http://www.apache.org/licenses/LICENSE-2.0
-#
-# Unless required by applicable law or agreed to in writing,
-# software distributed under the License is distributed on an
-# "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
-# KIND, either express or implied.  See the License for the
-# specific language governing permissions and limitations
-# under the License.
-
-
-def pytest_generate_tests(metafunc):
-    if "driver" in metafunc.fixturenames and metafunc.config.option.drivers:
-        metafunc.parametrize("driver", metafunc.config.option.drivers, indirect=True)
diff --git a/py/test/selenium/webdriver/common/conftest.py b/py/test/selenium/webdriver/common/conftest.py
deleted file mode 100644
index 043b7df7e146f..0000000000000
--- a/py/test/selenium/webdriver/common/conftest.py
+++ /dev/null
@@ -1,21 +0,0 @@
-# Licensed to the Software Freedom Conservancy (SFC) under one
-# or more contributor license agreements.  See the NOTICE file
-# distributed with this work for additional information
-# regarding copyright ownership.  The SFC licenses this file
-# to you under the Apache License, Version 2.0 (the
-# "License"); you may not use this file except in compliance
-# with the License.  You may obtain a copy of the License at
-#
-#   http://www.apache.org/licenses/LICENSE-2.0
-#
-# Unless required by applicable law or agreed to in writing,
-# software distributed under the License is distributed on an
-# "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
-# KIND, either express or implied.  See the License for the
-# specific language governing permissions and limitations
-# under the License.
-
-
-def pytest_generate_tests(metafunc):
-    if "driver" in metafunc.fixturenames and metafunc.config.option.drivers:
-        metafunc.parametrize("driver", metafunc.config.option.drivers, indirect=True)
diff --git a/py/test/selenium/webdriver/edge/conftest.py b/py/test/selenium/webdriver/edge/conftest.py
deleted file mode 100644
index 043b7df7e146f..0000000000000
--- a/py/test/selenium/webdriver/edge/conftest.py
+++ /dev/null
@@ -1,21 +0,0 @@
-# Licensed to the Software Freedom Conservancy (SFC) under one
-# or more contributor license agreements.  See the NOTICE file
-# distributed with this work for additional information
-# regarding copyright ownership.  The SFC licenses this file
-# to you under the Apache License, Version 2.0 (the
-# "License"); you may not use this file except in compliance
-# with the License.  You may obtain a copy of the License at
-#
-#   http://www.apache.org/licenses/LICENSE-2.0
-#
-# Unless required by applicable law or agreed to in writing,
-# software distributed under the License is distributed on an
-# "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
-# KIND, either express or implied.  See the License for the
-# specific language governing permissions and limitations
-# under the License.
-
-
-def pytest_generate_tests(metafunc):
-    if "driver" in metafunc.fixturenames and metafunc.config.option.drivers:
-        metafunc.parametrize("driver", metafunc.config.option.drivers, indirect=True)
diff --git a/py/test/selenium/webdriver/firefox/firefox_sizing_tests.py b/py/test/selenium/webdriver/firefox/firefox_sizing_tests.py
index fa417a3d782d7..ce157bd7edfb2 100644
--- a/py/test/selenium/webdriver/firefox/firefox_sizing_tests.py
+++ b/py/test/selenium/webdriver/firefox/firefox_sizing_tests.py
@@ -22,7 +22,6 @@
 import pytest
 
 from selenium import webdriver
-from selenium.webdriver.firefox.options import Options
 
 
 def is_running_wayland():
@@ -30,33 +29,20 @@ def is_running_wayland():
 
 
 @pytest.mark.skipif(not is_running_wayland(), reason="This test only runs on Linux under Wayland")
-def test_firefox_opens_large_when_running_xwayland(request):  # noqa: F821
-    options = Options()
-    if request.config.getoption("--headless"):
-        options.add_argument("-headless")
+def test_firefox_opens_large_when_running_xwayland(firefox_options):
     # setting environment variable `MOZ_ENABLE_WAYLAND=0` forces Firefox
     # to run under XWayland on Wayland based systems
     with patch.dict("os.environ", {"MOZ_ENABLE_WAYLAND": "0"}):
-        try:
-            driver = webdriver.Firefox(options=options)
+        with webdriver.Firefox(options=firefox_options) as driver:
             size = driver.get_window_size()
             assert size["height"] > 500
             assert size["width"] > 500
-        finally:
-            driver.quit()
 
 
 @pytest.mark.skipif(not is_running_wayland(), reason="This test only runs on Linux under Wayland")
 @pytest.mark.xfail(reason="https://bugzilla.mozilla.org/show_bug.cgi?id=1959040")
-# Firefox opens in a small window when running on Linux/Wayland
-def test_firefox_opens_large_when_running_wayland(request):  # noqa: F821
-    options = Options()
-    if request.config.getoption("--headless"):
-        options.add_argument("-headless")
-    try:
-        driver = webdriver.Firefox(options=options)
+def test_firefox_opens_large_when_running_wayland(firefox_options):
+    with webdriver.Firefox(options=firefox_options) as driver:
         size = driver.get_window_size()
         assert size["height"] > 500
         assert size["width"] > 500
-    finally:
-        driver.quit()
diff --git a/py/test/selenium/webdriver/remote/remote_connection_tests.py b/py/test/selenium/webdriver/remote/remote_connection_tests.py
index e4046aff719a4..438bc26cb0c42 100644
--- a/py/test/selenium/webdriver/remote/remote_connection_tests.py
+++ b/py/test/selenium/webdriver/remote/remote_connection_tests.py
@@ -14,12 +14,14 @@
 # KIND, either express or implied.  See the License for the
 # specific language governing permissions and limitations
 # under the License.
+
 import base64
 
 import filetype
 
 
 def test_browser_specific_method(driver, pages):
+    """This only works on Firefox"""
     pages.load("simpleTest.html")
     screenshot = driver.execute("FULL_PAGE_SCREENSHOT")["value"]
     result = base64.b64decode(screenshot)
diff --git a/py/test/selenium/webdriver/remote/custom_element_tests.py b/py/test/selenium/webdriver/remote/remote_custom_element_tests.py
similarity index 78%
rename from py/test/selenium/webdriver/remote/custom_element_tests.py
rename to py/test/selenium/webdriver/remote/remote_custom_element_tests.py
index 3fccb52ad3119..12a82e16fd79c 100644
--- a/py/test/selenium/webdriver/remote/custom_element_tests.py
+++ b/py/test/selenium/webdriver/remote/remote_custom_element_tests.py
@@ -14,6 +14,9 @@
 # KIND, either express or implied.  See the License for the
 # specific language governing permissions and limitations
 # under the License.
+
+import pytest
+
 from selenium.webdriver.common.by import By
 from selenium.webdriver.remote.webelement import WebElement
 
@@ -24,20 +27,27 @@ def custom_method(self):
         return "Custom element method"
 
 
-def test_find_element_with_custom_class(driver, pages):
+@pytest.fixture()
+def custom_element_driver(driver):
+    try:
+        driver._web_element_cls = MyCustomElement
+        yield driver
+    finally:
+        driver._web_element_cls = WebElement
+
+
+def test_find_element_with_custom_class(custom_element_driver, pages):
     """Test to ensure custom element class is used for a single element."""
-    driver._web_element_cls = MyCustomElement
     pages.load("simpleTest.html")
-    element = driver.find_element(By.TAG_NAME, "body")
+    element = custom_element_driver.find_element(By.TAG_NAME, "body")
     assert isinstance(element, MyCustomElement)
     assert element.custom_method() == "Custom element method"
 
 
-def test_find_elements_with_custom_class(driver, pages):
+def test_find_elements_with_custom_class(custom_element_driver, pages):
     """Test to ensure custom element class is used for multiple elements."""
-    driver._web_element_cls = MyCustomElement
     pages.load("simpleTest.html")
-    elements = driver.find_elements(By.TAG_NAME, "div")
+    elements = custom_element_driver.find_elements(By.TAG_NAME, "div")
     assert all(isinstance(el, MyCustomElement) for el in elements)
     assert all(el.custom_method() == "Custom element method" for el in elements)
 
diff --git a/py/test/selenium/webdriver/remote/remote_custom_locator_tests.py b/py/test/selenium/webdriver/remote/remote_custom_locator_tests.py
index e235f2ee2e999..efa0463148856 100644
--- a/py/test/selenium/webdriver/remote/remote_custom_locator_tests.py
+++ b/py/test/selenium/webdriver/remote/remote_custom_locator_tests.py
@@ -14,6 +14,10 @@
 # KIND, either express or implied.  See the License for the
 # specific language governing permissions and limitations
 # under the License.
+
+import pytest
+
+from selenium import webdriver
 from selenium.webdriver.remote.locator_converter import LocatorConverter
 
 
@@ -25,16 +29,25 @@ def convert(self, by, value):
         return super().convert(by, value)
 
 
-def test_find_element_with_custom_locator(driver):
-    driver.get("data:text/html,<div custom-attr='example'>Test</div>")
-    element = driver.find_element("custom", "example")
+@pytest.fixture()
+def custom_locator_driver(firefox_options):
+    driver = webdriver.Remote(options=firefox_options, locator_converter=CustomLocatorConverter())
+    yield driver
+    driver.quit()
+
+
+def test_find_element_with_custom_locator(custom_locator_driver):
+    custom_locator_driver.get("data:text/html,<div custom-attr='example'>Test</div>")
+    element = custom_locator_driver.find_element("custom", "example")
     assert element is not None
     assert element.text == "Test"
 
 
-def test_find_elements_with_custom_locator(driver):
-    driver.get("data:text/html,<div custom-attr='example'>Test1</div><div custom-attr='example'>Test2</div>")
-    elements = driver.find_elements("custom", "example")
+def test_find_elements_with_custom_locator(custom_locator_driver):
+    custom_locator_driver.get(
+        "data:text/html,<div custom-attr='example'>Test1</div><div custom-attr='example'>Test2</div>"
+    )
+    elements = custom_locator_driver.find_elements("custom", "example")
     assert len(elements) == 2
     assert elements[0].text == "Test1"
     assert elements[1].text == "Test2"
diff --git a/py/test/selenium/webdriver/remote/remote_downloads_tests.py b/py/test/selenium/webdriver/remote/remote_downloads_tests.py
index faa7fd996ecd8..5a8ed7f1fcbd4 100644
--- a/py/test/selenium/webdriver/remote/remote_downloads_tests.py
+++ b/py/test/selenium/webdriver/remote/remote_downloads_tests.py
@@ -14,6 +14,7 @@
 # KIND, either express or implied.  See the License for the
 # specific language governing permissions and limitations
 # under the License.
+
 import os
 import tempfile
 
diff --git a/py/test/selenium/webdriver/remote/remote_firefox_profile_tests.py b/py/test/selenium/webdriver/remote/remote_firefox_profile_tests.py
index 6d5c1d0cb54df..70b1d49b59be9 100644
--- a/py/test/selenium/webdriver/remote/remote_firefox_profile_tests.py
+++ b/py/test/selenium/webdriver/remote/remote_firefox_profile_tests.py
@@ -15,26 +15,13 @@
 # specific language governing permissions and limitations
 # under the License.
 
-import pytest
-
 from selenium import webdriver
+from selenium.webdriver.firefox.firefox_profile import FirefoxProfile
 
 
-@pytest.fixture
-def driver(options):
-    with pytest.warns(None) as record:
-        driver = webdriver.Remote(options=options)
-    assert len(record) == 0
-    yield driver
-    driver.quit()
-
-
-@pytest.fixture
-def options():
-    options = webdriver.FirefoxOptions()
-    options.set_preference("browser.startup.homepage", "about:")
-    return options
-
-
-def test_profile_is_used(driver):
-    assert "about:blank" == driver.current_url or "about:" == driver.current_url
+def test_profile_is_used(firefox_options):
+    ff_profile = FirefoxProfile()
+    ff_profile.set_preference("browser.startup.page", "1")
+    firefox_options.profile = ff_profile
+    with webdriver.Remote(options=firefox_options) as driver:
+        assert "browser/content/blanktab.html" in driver.current_url
diff --git a/py/test/selenium/webdriver/remote/remote_hub_connection.py b/py/test/selenium/webdriver/remote/remote_hub_connection.py
index 2a70fe0bad826..5540444b941fa 100644
--- a/py/test/selenium/webdriver/remote/remote_hub_connection.py
+++ b/py/test/selenium/webdriver/remote/remote_hub_connection.py
@@ -19,10 +19,14 @@
 import urllib3
 
 from selenium import webdriver
+from selenium.webdriver.firefox.options import Options
 
 
 def test_command_executor_ssl_certificate_is_verified():
+    options = Options()
+    site = "wrong.host.badssl.com"
     with pytest.raises(urllib3.exceptions.MaxRetryError) as excinfo:
-        webdriver.Remote(command_executor="https://wrong.host.badssl.com/")
+        webdriver.Remote(command_executor="https://wrong.host.badssl.com/", options=options)
     assert isinstance(excinfo.value.reason, urllib3.exceptions.SSLError)
-    assert "doesn't match" in str(excinfo.value)
+    assert site in str(excinfo.value)
+    assert "certificate is not valid" in str(excinfo.value).lower()
diff --git a/py/test/selenium/webdriver/support/conftest.py b/py/test/selenium/webdriver/support/conftest.py
deleted file mode 100644
index 043b7df7e146f..0000000000000
--- a/py/test/selenium/webdriver/support/conftest.py
+++ /dev/null
@@ -1,21 +0,0 @@
-# Licensed to the Software Freedom Conservancy (SFC) under one
-# or more contributor license agreements.  See the NOTICE file
-# distributed with this work for additional information
-# regarding copyright ownership.  The SFC licenses this file
-# to you under the Apache License, Version 2.0 (the
-# "License"); you may not use this file except in compliance
-# with the License.  You may obtain a copy of the License at
-#
-#   http://www.apache.org/licenses/LICENSE-2.0
-#
-# Unless required by applicable law or agreed to in writing,
-# software distributed under the License is distributed on an
-# "AS IS" BASIS, WITHOUT WARRANTIES OR CONDITIONS OF ANY
-# KIND, either express or implied.  See the License for the
-# specific language governing permissions and limitations
-# under the License.
-
-
-def pytest_generate_tests(metafunc):
-    if "driver" in metafunc.fixturenames and metafunc.config.option.drivers:
-        metafunc.parametrize("driver", metafunc.config.option.drivers, indirect=True)