diff --git a/lib/galaxy/selenium/navigates_galaxy.py b/lib/galaxy/selenium/navigates_galaxy.py
index a4e2a1c4bb9..e01bca9fbe0 100644
--- a/lib/galaxy/selenium/navigates_galaxy.py
+++ b/lib/galaxy/selenium/navigates_galaxy.py
@@ -1245,6 +1245,12 @@ class NavigatesGalaxy(HasDriver):
         self.driver.execute_script("arguments[0].scrollIntoView(true);", tool_element)
         tool_link.wait_for_and_click()
 
+    def datasource_tool_open(self, tool_id):
+        tool_link = self.components.tool_panel.data_source_tool_link(tool_id=tool_id)
+        tool_element = tool_link.wait_for_present()
+        self.driver.execute_script("arguments[0].scrollIntoView(true);", tool_element)
+        tool_link.wait_for_and_click()
+
     def tool_parameter_div(self, expanded_parameter_id):
         return self.components.tool_form.parameter_div(parameter=expanded_parameter_id).wait_for_clickable()
 
diff --git a/lib/galaxy/selenium/navigation.yml b/lib/galaxy/selenium/navigation.yml
index 0777d812704..cbe62a4dd9d 100644
--- a/lib/galaxy/selenium/navigation.yml
+++ b/lib/galaxy/selenium/navigation.yml
@@ -229,7 +229,7 @@ history_panel:
     refresh_button: '.history-refresh-button'
     name: '.title .name'
     name_beta: '.history-title span:last-child'
-    name_edit_input: 
+    name_edit_input:
       selector: 'name input'
       type: data-description
     contents: '#current-history-panel .history-content'
@@ -274,7 +274,7 @@ history_panel:
       selector: '//button[contains(span, "Return to legacy history panel")]'
     
     collection_menu_button: '.collection-menu'
-    collection_menu_edit_attributes: 
+    collection_menu_edit_attributes:
       type: xpath
       selector: '//button[@title="Edit attributes"]'
     new_history_button: '.history-new-button'
@@ -316,10 +316,10 @@ edit_dataset_attributes:
 
 edit_collection_attributes:
   selectors:
-    database_genome_tab: 
+    database_genome_tab:
       type: xpath
       selector: '//a[contains(text(), "Database/Build")]'
-    database_value: 
+    database_value:
       type: xpath
       selector: '//span[contains(text(), "${dbkey}")]'
     save_btn: '.save-collection-edit'
@@ -331,6 +331,7 @@ tool_panel:
   selectors:
     tool_link: 'a[href$$="tool_runner?tool_id=${tool_id}"]'
     outer_tool_link: '.toolTitle a[href$$="tool_runner?tool_id=${tool_id}"]'
+    data_source_tool_link: 'a[href$$="tool_runner/data_source_redirect?tool_id=${tool_id}"]'
     search: '.search-query'
     workflow_names: '#internal-workflows .toolTitle'
     views_button: '.tool-panel-dropdown'
diff --git a/lib/galaxy/webapps/base/webapp.py b/lib/galaxy/webapps/base/webapp.py
index 306f25db402..4835a5cd892 100644
--- a/lib/galaxy/webapps/base/webapp.py
+++ b/lib/galaxy/webapps/base/webapp.py
@@ -9,7 +9,10 @@ import socket
 import string
 import time
 from http.cookies import CookieError
-from typing import Any, Dict
+from typing import (
+    Any,
+    Dict,
+)
 from urllib.parse import urlparse
 
 import mako.lookup
@@ -63,6 +66,8 @@ UCSC_SERVERS = (
     'hgw8.soe.ucsc.edu',
 )
 
+TOOL_RUNNER_SESSION_COOKIE = "galaxytoolrunnersession"
+
 
 class WebApplication(base.WebApplication):
     """
@@ -379,14 +384,40 @@ class GalaxyWebTransaction(base.DefaultWebTransaction, context.ProvidesHistoryCo
             if name in self.response.cookies:
                 return self.response.cookies[name].value
             else:
+                if name not in self.request.cookies and TOOL_RUNNER_SESSION_COOKIE in self.request.cookies:
+                    # TOOL_RUNNER_SESSION_COOKIE value is the encoded galaxysession cookie.
+                    # We decode it here and pretend it's the galaxysession
+                    tool_runner_path = url_for(controller="tool_runner")
+                    if self.request.path.startswith(tool_runner_path):
+                        return self.security.decode_guid(self.request.cookies[TOOL_RUNNER_SESSION_COOKIE].value)
                 return self.request.cookies[name].value
         except Exception:
             return None
 
-    def set_cookie(self, value, name='galaxysession', path='/', age=90, version='1'):
+    def set_cookie(self, value, name="galaxysession", path="/", age=90, version="1"):
+        self._set_cookie(value, name=name, path=path, age=age, version=version)
+        if name == "galaxysession":
+            # Set an extra sessioncookie that will only be sent and be accepted on the tool_runner path.
+            # Use the id_secret to encode the sessioncookie, so if a malicious site
+            # obtains the sessioncookie they can only run tools.
+            self._set_cookie(
+                value,
+                name=TOOL_RUNNER_SESSION_COOKIE,
+                path=url_for(controller="tool_runner"),
+                age=age,
+                version=version,
+                encode_value=True,
+            )
+            tool_runner_cookie = self.response.cookies[TOOL_RUNNER_SESSION_COOKIE]
+            tool_runner_cookie["SameSite"] = "None"
+            tool_runner_cookie["secure"] = True
+
+    def _set_cookie(self, value, name="galaxysession", path="/", age=90, version="1", encode_value=False):
         """Convenience method for setting a session cookie"""
         # The galaxysession cookie value must be a high entropy 128 bit random number encrypted
         # using a server secret key.  Any other value is invalid and could pose security issues.
+        if encode_value:
+            value = self.security.encode_guid(value)
         self.response.cookies[name] = unicodify(value)
         self.response.cookies[name]['path'] = path
         self.response.cookies[name]['max-age'] = 3600 * 24 * age  # 90 days
diff --git a/lib/galaxy_test/api/test_authenticate.py b/lib/galaxy_test/api/test_authenticate.py
index 613fd80640d..479d22ea150 100644
--- a/lib/galaxy_test/api/test_authenticate.py
+++ b/lib/galaxy_test/api/test_authenticate.py
@@ -1,4 +1,5 @@
 import base64
+from urllib.parse import urljoin
 
 from requests import get
 
@@ -27,3 +28,29 @@ class AuthenticationApiTestCase(ApiTestCase):
         random_api_url = self._api_url("users", use_key=False)
         random_api_response = get(random_api_url, params=dict(key=auth_dict["api_key"]))
         self._assert_status_code_is(random_api_response, 200)
+
+    def test_tool_runner_session_cookie_handling(self):
+        response = get(self.url)
+        tool_runner_session_cookie = response.cookies["galaxytoolrunnersession"]
+        galaxy_session_cookie = response.cookies["galaxysession"]
+        assert tool_runner_session_cookie != galaxy_session_cookie
+        root_response = get(self.url, cookies={"galaxytoolrunnersession": tool_runner_session_cookie})
+        root_response.raise_for_status()
+        # Browser will only send cookie to /tool_runner path, but let's make sure it isn't accepted.
+        # Galaxy responds with a new session and sessioncookie in that case.
+        # (We might want to redirect to the login page instead if require_login is set?)
+        assert root_response.cookies["galaxysession"] != galaxy_session_cookie
+        tool_runner_response = get(
+            urljoin(self.url, "tool_runner?tool_id=test_data_source"),
+            cookies={"galaxytoolrunnersession": tool_runner_session_cookie},
+        )
+        tool_runner_response.raise_for_status()
+        # Verify that we're not returning the sessioncookie
+        assert "galaxysession" not in tool_runner_response.cookies
+        # Make sure history for original session received job
+        current_history_json_response = get(
+            urljoin(self.url, "history/current_history_json"), cookies={"galaxysession": galaxy_session_cookie}
+        )
+        current_history_json_response.raise_for_status()
+        current_history = current_history_json_response.json()
+        assert current_history["contents_active"]["active"] == 1
diff --git a/lib/galaxy_test/selenium/test_data_source_tools.py b/lib/galaxy_test/selenium/test_data_source_tools.py
new file mode 100644
index 00000000000..f537c6e20ae
--- /dev/null
+++ b/lib/galaxy_test/selenium/test_data_source_tools.py
@@ -0,0 +1,29 @@
+from galaxy_test.base.populators import skip_if_site_down
+from .framework import (
+    managed_history,
+    selenium_test,
+    SeleniumTestCase,
+    UsesHistoryItemAssertions,
+)
+
+
+class DataSourceTestCase(SeleniumTestCase, UsesHistoryItemAssertions):
+
+    ensure_registered = True
+
+    @selenium_test
+    @managed_history
+    @skip_if_site_down("https://genome.ucsc.edu/cgi-bin/hgTables")
+    def test_ucsc_table_direct1_data_source(self):
+        self.home()
+        self.datasource_tool_open("ucsc_table_direct1")
+        self.screenshot("ucsc_table_browser_first_page")
+        checkbox = self.wait_for_selector("#checkboxGalaxy")
+        assert checkbox.get_attribute("checked") == "true"
+        submit_button = self.wait_for_selector("#hgta_doTopSubmit")
+        submit_button.click()
+        self.screenshot("ucsc_table_browser_second_page")
+        self.wait_for_selector("#hgta_doGalaxyQuery").click()
+        self.history_panel_wait_for_hid_ok(1)
+        # Make sure we're still logged in (xref https://github.com/galaxyproject/galaxy/issues/11374)
+        self.components.masthead.logged_in_only.wait_for_visible()
diff --git a/test/functional/tools/samples_tool_conf.xml b/test/functional/tools/samples_tool_conf.xml
index cb29384d5c4..8eeb4238f5e 100644
--- a/test/functional/tools/samples_tool_conf.xml
+++ b/test/functional/tools/samples_tool_conf.xml
@@ -8,6 +8,7 @@
     <tool file="param_text_option.xml" />
     <tool file="column_param.xml" />
   </section>
+  <tool file="ucsc_tablebrowser.xml"/>
   <tool file="test_data_source.xml"/>
   <tool file="simple_constructs.xml" />
   <tool file="color_param.xml" />
diff --git a/test/functional/tools/ucsc_tablebrowser.xml b/test/functional/tools/ucsc_tablebrowser.xml
new file mode 120000
index 00000000000..ef273b19283
--- /dev/null
+++ b/test/functional/tools/ucsc_tablebrowser.xml
@@ -0,0 +1 @@
+../../../lib/galaxy/tools/bundled/data_source/ucsc_tablebrowser.xml
\ No newline at end of file