diff --git a/test/galaxy_selenium/cli.py b/test/galaxy_selenium/cli.py
index 93048dc26dc..e46a6f3a32a 100644
--- a/test/galaxy_selenium/cli.py
+++ b/test/galaxy_selenium/cli.py
@@ -3,7 +3,7 @@ BROWSER_DESCRIPTION = "Use specific browser for selenium (e.g. firefox or chrome
 REMOTE_HOST_DESCRIPTION = "Selenium hub remote host to use (if remote driver in use)."
 REMOTE_PORT_DESCRIPTION = "Selenium hub remote port to use (if remote driver in use)."
 GALAXY_URL_DESCRIPTION = "URL of Galaxy instance to target."
-HEADLESS_DESCRIPTION = "Use local selenium headlessly (requires pyvirtualdisplay)."
+HEADLESS_DESCRIPTION = "Use local selenium headlessly (native in chrome, otherwise this requires pyvirtualdisplay)."
 
 from six.moves.urllib.parse import urljoin
 
diff --git a/test/galaxy_selenium/driver_factory.py b/test/galaxy_selenium/driver_factory.py
index 1e9b729225c..8ddb0cd4953 100644
--- a/test/galaxy_selenium/driver_factory.py
+++ b/test/galaxy_selenium/driver_factory.py
@@ -6,6 +6,7 @@ except ImportError:
     Display = None
 
 from selenium import webdriver
+from selenium.webdriver.chrome.options import Options as ChromeOptions
 from selenium.webdriver.common.desired_capabilities import DesiredCapabilities
 
 
@@ -15,15 +16,18 @@ LOGGING_PREFS = {
 }
 
 
-def get_local_driver(browser=DEFAULT_BROWSER):
+def get_local_browser(browser):
     if browser == "auto":
         if _which("chromedriver"):
-            browser = "CHROME"
+            return "CHROME"
         elif _which("geckodriver"):
-            browser = "FIREFOX"
+            return "FIREFOX"
         else:
             raise Exception("Selenium browser is 'auto' but neither geckodriver or chromedriver are found on PATH.")
 
+
+def get_local_driver(browser=DEFAULT_BROWSER, headless=False):
+    browser = get_local_browser(browser)
     assert browser in ["CHROME", "FIREFOX", "OPERA", "PHANTOMJS"]
     driver_to_class = {
         "CHROME": webdriver.Chrome,
@@ -32,7 +36,12 @@ def get_local_driver(browser=DEFAULT_BROWSER):
         "PHANTOMJS": webdriver.PhantomJS,
     }
     driver_class = driver_to_class[browser]
-    return driver_class(desired_capabilities={"loggingPrefs": LOGGING_PREFS})
+    if browser == 'CHROME' and headless:
+        options = ChromeOptions()
+        options.add_argument('--headless')
+        return driver_class(desired_capabilities={"loggingPrefs": LOGGING_PREFS}, chrome_options=options)
+    else:
+        return driver_class(desired_capabilities={"loggingPrefs": LOGGING_PREFS})
 
 
 def get_remote_driver(
diff --git a/test/galaxy_selenium/navigates_galaxy.py b/test/galaxy_selenium/navigates_galaxy.py
index 3856880a246..f3bc993bf91 100644
--- a/test/galaxy_selenium/navigates_galaxy.py
+++ b/test/galaxy_selenium/navigates_galaxy.py
@@ -1257,7 +1257,7 @@ class NavigatesGalaxy(HasDriver):
             self.home()
             self.click_masthead_user()
             self.wait_for_and_click(self.navigation.masthead.labels.logout)
-            self.click_label('go to the home page')
+            self.sleep_for(WAIT_TYPES.UX_TRANSITION)
             assert not self.is_logged_in()
 
     def run_tour(self, path, skip_steps=None, sleep_on_steps=None, tour_callback=None):
diff --git a/test/selenium_tests/framework.py b/test/selenium_tests/framework.py
index d0166dcd846..480b9e801d8 100644
--- a/test/selenium_tests/framework.py
+++ b/test/selenium_tests/framework.py
@@ -287,7 +287,7 @@ class SeleniumTestCase(FunctionalTestCase, NavigatesGalaxy, UsesApiTestCaseMixin
         self._try_setup_with_driver()
 
     def setup_driver_and_session(self):
-        self.display = driver_factory.virtual_display_if_enabled(headless_selenium())
+        self.display = driver_factory.virtual_display_if_enabled(use_virtual_display())
         self.driver = get_driver()
         # New workflow index page does not degrade well to smaller sizes, needed
         # to increase this.
@@ -488,7 +488,20 @@ def headless_selenium():
         return False
 
     if GALAXY_TEST_SELENIUM_HEADLESS == "auto":
-        if driver_factory.is_virtual_display_available():
+        if driver_factory.is_virtual_display_available() or driver_factory.get_local_browser(GALAXY_TEST_SELENIUM_BROWSER) == "CHROME":
+            return True
+        else:
+            return False
+    else:
+        return asbool(GALAXY_TEST_SELENIUM_HEADLESS)
+
+
+def use_virtual_display():
+    if asbool(GALAXY_TEST_SELENIUM_REMOTE):
+        return False
+
+    if GALAXY_TEST_SELENIUM_HEADLESS == "auto":
+        if driver_factory.is_virtual_display_available() and not driver_factory.get_local_browser(GALAXY_TEST_SELENIUM_BROWSER) == "CHROME":
             return True
         else:
             return False
@@ -497,7 +510,10 @@ def headless_selenium():
 
 
 def get_local_driver():
-    return driver_factory.get_local_driver(GALAXY_TEST_SELENIUM_BROWSER)
+    return driver_factory.get_local_driver(
+        GALAXY_TEST_SELENIUM_BROWSER,
+        headless_selenium()
+    )
 
 
 def get_remote_driver():