diff --git a/app/__init__.py b/app/__init__.py
index 0eb444f53..d064906f8 100644
--- a/app/__init__.py
+++ b/app/__init__.py
@@ -39,7 +39,7 @@ from werkzeug.local import LocalProxy
 from app import proxy_fix
 from app.config import configs
 from app.asset_fingerprinter import AssetFingerprinter
-from app.navigation import MainNavigation
+from app.navigation import HeaderNavigation, MainNavigation
 from app.notify_client.service_api_client import ServiceAPIClient
 from app.notify_client.api_key_api_client import ApiKeyApiClient
 from app.notify_client.invite_api_client import InviteApiClient
@@ -90,7 +90,10 @@ current_service = LocalProxy(partial(_lookup_req_object, 'service'))
 # The current organisation attached to the request stack.
 current_organisation = LocalProxy(partial(_lookup_req_object, 'organisation'))
 
-main_navigation = MainNavigation()
+navigation = {
+    'main_navigation': MainNavigation(),
+    'header_navigation': HeaderNavigation(),
+}
 
 
 def create_app(application):
@@ -176,7 +179,7 @@ def init_app(application):
 
     @application.context_processor
     def _nav_selected():
-        return {'main_navigation': main_navigation}
+        return navigation
 
     @application.before_request
     def record_start_time():
diff --git a/app/navigation.py b/app/navigation.py
index 78bd6b102..6440d5357 100644
--- a/app/navigation.py
+++ b/app/navigation.py
@@ -7,6 +7,7 @@ class Navigation:
 
     mapping = {}
     exclude = {}
+    selected_attribute = "class=selected"
 
     def __init__(self):
         self.mapping = {
@@ -30,10 +31,232 @@ class Navigation:
 
     def is_selected(self, navigation_item):
         if request.endpoint in self.mapping[navigation_item]:
-            return "class=selected"
+            return self.selected_attribute
         return ''
 
 
+class HeaderNavigation(Navigation):
+
+    selected_attribute = "class=active"
+
+    mapping = {
+        'support': {
+            'bat_phone',
+            'feedback',
+            'old_feedback',
+            'old_submit_feedback',
+            'support',
+            'thanks',
+            'triage',
+        },
+        'features': {
+            'features',
+            'roadmap',
+            'security',
+            'terms',
+            'using_notify',
+        },
+        'pricing': {
+            'pricing',
+        },
+        'documentation': {
+            'documentation',
+            'integration_testing',
+        },
+        'user-profile': {
+            'user_profile',
+            'user_profile_email',
+            'user_profile_email_authenticate',
+            'user_profile_email_confirm',
+            'user_profile_mobile_number',
+            'user_profile_mobile_number_authenticate',
+            'user_profile_mobile_number_confirm',
+            'user_profile_name',
+            'user_profile_password',
+        },
+        'platform-admin': {
+            'add_organisation',
+            'create_email_branding',
+            'email_branding',
+            'live_services',
+            'organisations',
+            'platform_admin',
+            'suspend_service',
+            'trial_services',
+            'update_email_branding',
+            'view_provider',
+            'view_providers',
+        },
+        'sign-in': {
+            'sign_in',
+            'two_factor',
+            'two_factor_email',
+            'two_factor_email_sent',
+            'verify',
+            'verify_email',
+            'verify_mobile',
+        },
+    }
+
+    exclude = {
+        'accept_invite',
+        'accept_org_invite',
+        'action_blocked',
+        'add_service',
+        'add_service_template',
+        'add_template_by_type',
+        'agreement',
+        'api_callbacks',
+        'api_documentation',
+        'api_integration',
+        'api_keys',
+        'archive_service',
+        'callbacks',
+        'cancel_invited_org_user',
+        'cancel_invited_user',
+        'cancel_job',
+        'check_and_resend_text_code',
+        'check_and_resend_verification_code',
+        'check_messages',
+        'check_messages_preview',
+        'check_notification',
+        'choose_account',
+        'choose_service',
+        'choose_template',
+        'confirm_edit_organisation_name',
+        'confirm_redact_template',
+        'conversation',
+        'conversation_reply',
+        'conversation_reply_with_template',
+        'conversation_updates',
+        'cookies',
+        'create_api_key',
+        'delete_service_template',
+        'delivery_and_failure',
+        'delivery_status_callback',
+        'design_content',
+        'download_agreement',
+        'download_notifications_csv',
+        'edit_organisation_name',
+        'edit_provider',
+        'edit_service_template',
+        'edit_user_org_permissions',
+        'edit_user_permissions',
+        'email_not_received',
+        'email_template',
+        'error',
+        'forgot_password',
+        'get_example_csv',
+        'get_notifications_as_json',
+        'go_to_dashboard_after_tour',
+        'inbound_sms_admin',
+        'inbox',
+        'inbox_download',
+        'inbox_updates',
+        'index',
+        'information_risk_management',
+        'information_security',
+        'invite_org_user',
+        'invite_user',
+        'letter_jobs',
+        'link_service_to_organisation',
+        'manage_org_users',
+        'manage_users',
+        'monthly',
+        'new_password',
+        'old_integration_testing',
+        'old_roadmap',
+        'old_service_dashboard',
+        'old_terms',
+        'old_using_notify',
+        'organisation_dashboard',
+        'organisation_settings',
+        'received_text_messages_callback',
+        'redact_template',
+        'register',
+        'register_from_invite',
+        'register_from_org_invite',
+        'registration_continue',
+        'remove_user_from_organisation',
+        'remove_user_from_service',
+        'request_to_go_live',
+        'resend_email_link',
+        'resend_email_verification',
+        'resume_service',
+        'revoke_api_key',
+        'send_messages',
+        'send_notification',
+        'send_one_off',
+        'send_one_off_step',
+        'send_test',
+        'send_test_preview',
+        'send_test_step',
+        'service_add_email_reply_to',
+        'service_add_letter_contact',
+        'service_add_sms_sender',
+        'service_dashboard',
+        'service_dashboard_updates',
+        'service_edit_email_reply_to',
+        'service_edit_letter_contact',
+        'service_edit_sms_sender',
+        'service_email_reply_to',
+        'service_letter_contact_details',
+        'service_name_change',
+        'service_name_change_confirm',
+        'service_set_auth_type',
+        'service_set_email',
+        'service_set_email_branding',
+        'service_set_inbound_number',
+        'service_set_inbound_sms',
+        'service_set_international_sms',
+        'service_set_letter_contact_block',
+        'service_set_letters',
+        'service_set_reply_to_email',
+        'service_set_sms',
+        'service_set_sms_prefix',
+        'service_settings',
+        'service_sms_senders',
+        'service_switch_can_send_email',
+        'service_switch_can_send_precompiled_letter',
+        'service_switch_can_send_sms',
+        'service_switch_email_auth',
+        'service_switch_live',
+        'service_switch_research_mode',
+        'services_or_dashboard',
+        'set_free_sms_allowance',
+        'set_letter_branding',
+        'set_organisation_type',
+        'set_sender',
+        'set_template_sender',
+        'show_accounts_or_dashboard',
+        'sign_out',
+        'start_job',
+        'start_tour',
+        'styleguide',
+        'submit_request_to_go_live',
+        'temp_service_history',
+        'template_history',
+        'template_usage',
+        'trial_mode',
+        'usage',
+        'view_job',
+        'view_job_csv',
+        'view_job_updates',
+        'view_jobs',
+        'view_letter_notification_as_preview',
+        'view_letter_template_preview',
+        'view_notification',
+        'view_notification_updates',
+        'view_notifications',
+        'view_notifications_csv',
+        'view_template',
+        'view_template_version',
+        'view_template_version_preview',
+        'view_template_versions',
+        'whitelist',
+    }
+
+
 class MainNavigation(Navigation):
 
     mapping = {
diff --git a/app/templates/admin_template.html b/app/templates/admin_template.html
index 6595057e7..d8c1c8ca7 100644
--- a/app/templates/admin_template.html
+++ b/app/templates/admin_template.html
@@ -40,19 +40,19 @@
       <a href="#proposition-links" class="js-header-toggle menu">Menu</a>
       <nav id="proposition-menu">
         <ul id="proposition-links">
-          <li><a href="{{ url_for('main.support') }}">Support</a></li>
+          <li><a href="{{ url_for('main.support') }}" {{ header_navigation.is_selected('support') }}>Support</a></li>
           {% if current_user.is_authenticated %}
-            <li><a href="{{ url_for('main.documentation') }}">Documentation</a></li>
-            <li><a href="{{ url_for('main.user_profile') }}">{{ current_user.name }}</a></li>
+            <li><a href="{{ url_for('main.documentation') }}" {{ header_navigation.is_selected('documentation') }}>Documentation</a></li>
+            <li><a href="{{ url_for('main.user_profile') }}" {{ header_navigation.is_selected('user-profile') }}>{{ current_user.name }}</a></li>
             {% if current_user.platform_admin %}
-              <li><a href="{{ url_for('main.platform_admin') }}">Platform admin</a></li>
+              <li><a href="{{ url_for('main.platform_admin') }}" {{ header_navigation.is_selected('platform-admin') }}>Platform admin</a></li>
             {% endif %}
             <li><a href="{{ url_for('main.sign_out')}}">Sign out</a></li>
           {% else %}
-            <li><a href="{{ url_for('main.features') }}">Features</a></li>
-            <li><a href="{{ url_for('main.pricing' )}}">Pricing</a></li>
-            <li><a href="{{ url_for('main.documentation') }}">Documentation</a></li>
-            <li><a href="{{ url_for('main.sign_in' )}}">Sign in</a></li>
+            <li><a href="{{ url_for('main.features') }}" {{ header_navigation.is_selected('features') }}>Features</a></li>
+            <li><a href="{{ url_for('main.pricing' )}}" {{ header_navigation.is_selected('pricing') }}>Pricing</a></li>
+            <li><a href="{{ url_for('main.documentation') }}" {{ header_navigation.is_selected('documentation') }}>Documentation</a></li>
+            <li><a href="{{ url_for('main.sign_in' )}}" {{ header_navigation.is_selected('sign-in') }}>Sign in</a></li>
           {% endif %}
         </ul>
       </nav>
diff --git a/tests/app/test_navigation.py b/tests/app/test_navigation.py
index acbfcb6de..4388a9719 100644
--- a/tests/app/test_navigation.py
+++ b/tests/app/test_navigation.py
@@ -1,38 +1,91 @@
 import pytest
 from tests.conftest import SERVICE_ONE_ID, app_
 
-from app.navigation import MainNavigation
+from app.navigation import HeaderNavigation, MainNavigation
 
 all_endpoints = [
     rule.endpoint for rule in next(app_(None)).url_map.iter_rules()
 ]
 
 
-def test_navigation_items_are_properly_defined():
-    for endpoint in MainNavigation().endpoints_with_navigation:
-        assert endpoint in all_endpoints
-        assert endpoint not in MainNavigation().endpoints_without_navigation
-        assert MainNavigation().endpoints_with_navigation.count(endpoint) == 1
-
-
-def test_excluded_navigation_items_are_properly_defined():
-    for endpoint in MainNavigation().endpoints_without_navigation:
-        assert endpoint in all_endpoints
-        assert endpoint not in MainNavigation().endpoints_with_navigation
-        assert MainNavigation().endpoints_without_navigation.count(endpoint) == 1
-
-
-def test_all_endpoints_are_covered():
-    for endpoint in all_endpoints:
-        assert endpoint in (
-            MainNavigation().endpoints_with_navigation +
-            MainNavigation().endpoints_without_navigation
+@pytest.mark.parametrize('navigation_instance', [
+    MainNavigation(),
+    HeaderNavigation(),
+])
+def test_navigation_items_are_properly_defined(navigation_instance):
+    for endpoint in navigation_instance.endpoints_with_navigation:
+        assert (
+            endpoint in all_endpoints
+        ), '{} is not a real endpoint (in {}.mapping)'.format(
+            endpoint,
+            type(navigation_instance).__name__
+        )
+        assert (
+            endpoint not in navigation_instance.endpoints_without_navigation
+        ), '{} is listed in {}.mapping and {}.exclude'.format(
+            endpoint,
+            type(navigation_instance).__name__,
+            type(navigation_instance).__name__,
+        )
+        assert (
+            navigation_instance.endpoints_with_navigation.count(endpoint) == 1
+        ), '{} found more than once in {}.mapping'.format(
+            endpoint,
+            type(navigation_instance).__name__
         )
 
 
+@pytest.mark.parametrize('navigation_instance', [
+    MainNavigation(),
+    HeaderNavigation(),
+])
+def test_excluded_navigation_items_are_properly_defined(navigation_instance):
+    for endpoint in navigation_instance.endpoints_without_navigation:
+        assert (
+            endpoint in all_endpoints
+        ), '{} is not a real endpoint (in {}.exclude)'.format(
+            endpoint,
+            type(navigation_instance).__name__
+        )
+        assert (
+            endpoint not in navigation_instance.endpoints_with_navigation
+        ), '{} is listed in {}.exclude and {}.mapping'.format(
+            endpoint,
+            type(navigation_instance).__name__,
+            type(navigation_instance).__name__,
+        )
+        assert (
+            navigation_instance.endpoints_without_navigation.count(endpoint) == 1
+        ), '{} found more than once in {}.exclude'.format(
+            endpoint,
+            type(navigation_instance).__name__
+        )
+
+
+@pytest.mark.parametrize('navigation_instance', [
+    MainNavigation(),
+    HeaderNavigation(),
+])
+def test_all_endpoints_are_covered(navigation_instance):
+    for endpoint in all_endpoints:
+        assert endpoint in (
+            navigation_instance.endpoints_with_navigation +
+            navigation_instance.endpoints_without_navigation
+        ), '{} is not listed or excluded in {}'.format(
+            endpoint,
+            type(navigation_instance).__name__
+        )
+
+
+@pytest.mark.parametrize('navigation_instance', [
+    MainNavigation(),
+    HeaderNavigation(),
+])
 @pytest.mark.xfail(raises=KeyError)
-def test_raises_on_invalid_navigation_item(client_request):
-    MainNavigation().is_selected('foo')
+def test_raises_on_invalid_navigation_item(
+    client_request, navigation_instance
+):
+    navigation_instance.is_selected('foo')
 
 
 @pytest.mark.parametrize('endpoint, selected_nav_item', [
@@ -51,3 +104,18 @@ def test_a_page_should_nave_selected_navigation_item(
     selected_nav_items = page.select('.navigation a.selected')
     assert len(selected_nav_items) == 1
     assert selected_nav_items[0].text.strip() == selected_nav_item
+
+
+@pytest.mark.parametrize('endpoint, selected_nav_item', [
+    ('main.documentation', 'Documentation'),
+    ('main.support', 'Support'),
+])
+def test_a_page_should_nave_selected_header_navigation_item(
+    client_request,
+    endpoint,
+    selected_nav_item,
+):
+    page = client_request.get(endpoint, service_id=SERVICE_ONE_ID)
+    selected_nav_items = page.select('#proposition-links a.active')
+    assert len(selected_nav_items) == 1
+    assert selected_nav_items[0].text.strip() == selected_nav_item