diff --git a/apps/docs/features/docs/Reference.apiPage.tsx b/apps/docs/features/docs/Reference.apiPage.tsx
index e8344cb3a85..e1deb6ae802 100644
--- a/apps/docs/features/docs/Reference.apiPage.tsx
+++ b/apps/docs/features/docs/Reference.apiPage.tsx
@@ -27,21 +27,22 @@ async function ApiOperationPage({ operationSlug }: { operationSlug: string }) {
   const section = sectionsBySlug?.get(operationSlug)
   if (!section) notFound()
 
+  const navigationProps = {
+    libraryId: 'api',
+    name: 'Management API',
+    menuData: reference_api,
+    libPath: 'api',
+    version: 'latest',
+    isLatestVersion: true,
+    realNavigation: true,
+  }
+
   return (
     <ReferenceContentScrollHandler libPath="api" version="latest" isLatestVersion={true}>
       <SidebarSkeleton
         menuId={MenuId.RefApi}
-        NavigationMenu={
-          <ReferenceNavigation
-            libraryId="api"
-            name="Management API"
-            menuData={reference_api}
-            libPath="api"
-            version="latest"
-            isLatestVersion={true}
-            realNavigation
-          />
-        }
+        NavigationMenu={<ReferenceNavigation {...navigationProps} />}
+        rightRail={<ReferenceNavigation {...navigationProps} hasActiveCrumb />}
       >
         <LayoutMainContent>
           <article className="@container/article">
diff --git a/apps/docs/features/docs/Reference.cliPage.tsx b/apps/docs/features/docs/Reference.cliPage.tsx
index 9d549b5d858..aca9c394c23 100644
--- a/apps/docs/features/docs/Reference.cliPage.tsx
+++ b/apps/docs/features/docs/Reference.cliPage.tsx
@@ -8,20 +8,21 @@ import { LayoutMainContent } from '~/layouts/DefaultLayout'
 import { SidebarSkeleton } from '~/layouts/MainSkeleton'
 
 export async function CliReferencePage() {
+  const navigationProps = {
+    libraryId: 'cli',
+    name: 'Supabase CLI',
+    menuData: reference_cli,
+    libPath: 'cli',
+    version: 'latest',
+    isLatestVersion: true,
+  }
+
   return (
     <ReferenceContentScrollHandler libPath="cli" version="latest" isLatestVersion={true}>
       <SidebarSkeleton
         menuId={MenuId.RefCli}
-        NavigationMenu={
-          <ReferenceNavigation
-            libraryId="cli"
-            name="Supabase CLI"
-            menuData={reference_cli}
-            libPath="cli"
-            version="latest"
-            isLatestVersion={true}
-          />
-        }
+        NavigationMenu={<ReferenceNavigation {...navigationProps} />}
+        rightRail={<ReferenceNavigation {...navigationProps} hasActiveCrumb />}
       >
         <LayoutMainContent>
           <article className="@container/article">
diff --git a/apps/docs/features/docs/Reference.navigation.client.tsx b/apps/docs/features/docs/Reference.navigation.client.tsx
index 18dd75f8d65..9a418fefa9a 100644
--- a/apps/docs/features/docs/Reference.navigation.client.tsx
+++ b/apps/docs/features/docs/Reference.navigation.client.tsx
@@ -7,6 +7,7 @@ import {
 } from '~/components/Navigation/NavSection'
 import type { AbbrevApiReferenceSection } from '~/features/docs/Reference.utils'
 import { isElementInViewport } from '~/features/ui/helpers.dom'
+import { HeadingSlotCrumb } from '~/layouts/HeadingSlot'
 import { BASE_PATH } from '~/lib/constants'
 import { debounce } from 'lodash-es'
 import Link from 'next/link'
@@ -25,6 +26,19 @@ import {
 } from 'react'
 import { cn } from 'ui'
 
+export interface ReferenceCrumbHeading {
+  url: string
+  title: string
+}
+
+interface ReferenceActiveCrumbProps {
+  basePath: string
+  headings: ReferenceCrumbHeading[]
+}
+
+export const ACTIVE_BAR_CLASS_NAME =
+  'aria-[current=page]:before:absolute aria-[current=page]:before:-left-[13px] aria-[current=page]:before:top-1/2 aria-[current=page]:before:h-[1em] aria-[current=page]:before:w-px aria-[current=page]:before:-translate-y-1/2 aria-[current=page]:before:bg-brand'
+
 export const ReferenceContentInitiallyScrolledContext = createContext<boolean>(false)
 
 let patchCount = 0
@@ -126,38 +140,27 @@ export function ReferenceContentScrollHandler({
 export function ReferenceNavigationScrollHandler({
   children,
   ...rest
-}: PropsWithChildren & HTMLAttributes<HTMLDivElement>) {
-  const parentRef = useRef<HTMLElement | null>(null)
-  const ref = useRef<HTMLDivElement | null>(null)
+}: PropsWithChildren & HTMLAttributes<HTMLElement>) {
+  const ref = useRef<HTMLElement | null>(null)
   const initialScrollHappened = useContext(ReferenceContentInitiallyScrolledContext)
 
-  useEffect(() => {
-    if (!ref.current) return
+  const scrollActiveIntoView = useCallback(() => {
+    if (!ref.current?.offsetParent) return
+
+    const currentLink = ref.current.querySelector<HTMLElement>('[aria-current=page]')
+    if (!currentLink || isElementInViewport(currentLink)) return
 
     let scrollingParent: HTMLElement = ref.current
-
-    while (scrollingParent && !(scrollingParent.scrollHeight > scrollingParent.clientHeight)) {
-      const parent = scrollingParent.parentElement
-      if (!parent) break
-      scrollingParent = parent
+    while (scrollingParent.scrollHeight <= scrollingParent.clientHeight) {
+      if (!scrollingParent.parentElement) return
+      scrollingParent = scrollingParent.parentElement
     }
 
-    parentRef.current = scrollingParent
-  }, [])
-
-  const scrollActiveIntoView = useCallback(() => {
-    const currentLink = ref.current?.querySelector('[aria-current=page]') as HTMLElement
-    if (currentLink && !isElementInViewport(currentLink)) {
-      // Calculate the offset of the current link relative to scrollingParent
-      // and scroll the parent to the top of the link.
-      const offsetTop = currentLink.offsetTop
-      const parentOffsetTop = parentRef.current?.offsetTop ?? 0
-      const scrollPosition = offsetTop - parentOffsetTop
-
-      parentRef.current?.scrollTo({
-        top: scrollPosition - 60 /* space for header + padding */,
-      })
-    }
+    const linkOffset =
+      currentLink.getBoundingClientRect().top - scrollingParent.getBoundingClientRect().top
+    scrollingParent.scrollTo({
+      top: scrollingParent.scrollTop + linkOffset - 60 /* space for header + padding */,
+    })
   }, [])
 
   useEffect(() => {
@@ -174,9 +177,9 @@ export function ReferenceNavigationScrollHandler({
   }, [scrollActiveIntoView])
 
   return (
-    <div ref={ref} {...rest}>
+    <nav ref={ref} {...rest}>
       {children}
-    </div>
+    </nav>
   )
 }
 
@@ -184,12 +187,19 @@ function deriveHref(basePath: string, section: AbbrevApiReferenceSection) {
   return 'slug' in section ? `${basePath}/${section.slug}` : ''
 }
 
-function getLinkStyles(isActive: boolean, className?: string) {
+export function ReferenceActiveCrumb({ basePath, headings }: ReferenceActiveCrumbProps) {
+  const pathname = useCurrentPathname()
+  const activePath = pathname === basePath ? `${basePath}/introduction` : pathname
+  const index = headings.findIndex((heading) => heading.url === activePath)
+
+  return <HeadingSlotCrumb heading={headings[index]} index={index} />
+}
+
+function getLinkStyles(className?: string) {
   return cn(
-    'text-sm text-foreground-lighter',
-    !isActive && 'hover:text-foreground',
-    isActive && 'text-primary',
-    'transition-colors',
+    'relative block py-1 text-sm text-foreground-lighter wrap-anywhere',
+    'transition-colors duration-150 hover:text-foreground-light',
+    'aria-[current=page]:text-foreground',
     className
   )
 }
@@ -264,9 +274,8 @@ export function RefLink({
   useEffect(() => {
     if (ref.current) {
       ref.current.ariaCurrent = isActive ? 'page' : null
-      ref.current.className = getLinkStyles(isActive, className)
     }
-  }, [isActive, className])
+  }, [isActive])
 
   const onClick = useCallback(
     (evt: MouseEvent) => {
@@ -292,7 +301,7 @@ export function RefLink({
           // pages omit the prop and keep Next.js's default prefetch behavior.
           {...(!realNavigation ? { prefetch: false } : {})}
           href={href}
-          className={getLinkStyles(isActive, className)}
+          className={getLinkStyles(className)}
           onClick={onClick}
         >
           {section.title}
@@ -353,7 +362,7 @@ function CompoundRefLink({
             'flex items-center justify-between gap-2'
           )}
         >
-          <span className={getLinkStyles(false)}>{section.title}</span>
+          <span className={getLinkStyles()}>{section.title}</span>
           <NavSectionCaret className="group-disabled:cursor-not-allowed group-disabled:opacity-10" />
         </button>
       </Collapsible.Trigger>
@@ -366,7 +375,7 @@ function CompoundRefLink({
                   <RefLink
                     basePath={basePath}
                     section={item}
-                    className="block py-1.25"
+                    className={ACTIVE_BAR_CLASS_NAME}
                     realNavigation={realNavigation}
                   />
                 </li>
diff --git a/apps/docs/features/docs/Reference.navigation.tsx b/apps/docs/features/docs/Reference.navigation.tsx
index 393624245c3..08dd10c29fe 100644
--- a/apps/docs/features/docs/Reference.navigation.tsx
+++ b/apps/docs/features/docs/Reference.navigation.tsx
@@ -1,16 +1,15 @@
-import { isFeatureEnabled } from 'common'
-import { type PropsWithChildren } from 'react'
-
-import { cn } from 'ui'
-
 import MenuIconPicker from '~/components/Navigation/NavigationMenu/MenuIconPicker'
 import RefVersionDropdown from '~/components/RefVersionDropdown'
 import { getReferenceSections } from '~/features/docs/Reference.generated.singleton'
 import {
-  RefLink,
+  ACTIVE_BAR_CLASS_NAME,
+  ReferenceActiveCrumb,
   ReferenceNavigationScrollHandler,
+  RefLink,
+  type ReferenceCrumbHeading,
 } from '~/features/docs/Reference.navigation.client'
 import { type AbbrevApiReferenceSection } from '~/features/docs/Reference.utils'
+import { isFeatureEnabled } from 'common'
 
 interface ReferenceNavigationProps {
   libraryId: string
@@ -23,8 +22,27 @@ interface ReferenceNavigationProps {
   // instead of scrolling within one giant page. SDK/CLI/self-hosting callers
   // never pass this, so their behavior is unchanged.
   realNavigation?: boolean
+  // only one of the two rendered copies owns the header crumb
+  hasActiveCrumb?: boolean
 }
 
+interface RefCategoryProps {
+  basePath: string
+  section: AbbrevApiReferenceSection
+  realNavigation?: boolean
+}
+
+const flattenSections = (sections: AbbrevApiReferenceSection[]): AbbrevApiReferenceSection[] =>
+  sections.flatMap((section) => [section, ...flattenSections(section.items ?? [])])
+
+const getCrumbHeadings = (basePath: string, sections: AbbrevApiReferenceSection[]) =>
+  flattenSections(sections).reduce<ReferenceCrumbHeading[]>((headings, section) => {
+    if (section.slug && section.title) {
+      headings.push({ url: `${basePath}/${section.slug}`, title: section.title })
+    }
+    return headings
+  }, [])
+
 export async function ReferenceNavigation({
   libraryId,
   name,
@@ -33,6 +51,7 @@ export async function ReferenceNavigation({
   version,
   isLatestVersion,
   realNavigation,
+  hasActiveCrumb = false,
 }: ReferenceNavigationProps) {
   const navSections = await getReferenceSections(libraryId, version)
   const filteredNavSections = navSections?.filter((section) => section.title !== 'Auth')
@@ -41,20 +60,31 @@ export async function ReferenceNavigation({
   const basePath = `/reference/${libPath}${isLatestVersion ? '' : `/${version}`}`
 
   return (
-    <ReferenceNavigationScrollHandler className="w-full flex flex-col pt-3 pb-5 gap-3">
-      <div className="flex items-center gap-3">
-        {'icon' in menuData && <MenuIconPicker icon={menuData.icon || ''} width={21} height={21} />}
-        <span className="text-base text-brand-600">{name}</span>
+    <ReferenceNavigationScrollHandler
+      aria-label={`${name} reference`}
+      className="w-full flex flex-col gap-4"
+    >
+      {hasActiveCrumb && displayedNavSections ? (
+        <ReferenceActiveCrumb
+          basePath={basePath}
+          headings={getCrumbHeadings(basePath, displayedNavSections)}
+        />
+      ) : null}
+      <div className="flex items-center gap-2">
+        {'icon' in menuData ? (
+          <MenuIconPicker icon={menuData.icon || ''} width={16} height={16} />
+        ) : null}
+        <span className="text-sm font-medium text-foreground">{name}</span>
         <RefVersionDropdown library={libPath} currentVersion={version} />
       </div>
-      <ul className="flex flex-col gap-2">
-        {displayedNavSections?.map((section, index) =>
+      <ul className="flex flex-col gap-1">
+        {displayedNavSections?.map((section) =>
           section.type === 'category' ? (
-            <li key={section.id ?? String(index)}>
+            <li key={section.id}>
               <RefCategory basePath={basePath} section={section} realNavigation={realNavigation} />
             </li>
           ) : (
-            <li key={section.id ?? String(index)} className={topLvlRefNavItemStyles}>
+            <li key={section.id}>
               <RefLink basePath={basePath} section={section} realNavigation={realNavigation} />
             </li>
           )
@@ -64,47 +94,28 @@ export async function ReferenceNavigation({
   )
 }
 
-const topLvlRefNavItemStyles = 'leading-5'
-
-function RefCategory({
-  basePath,
-  section,
-  realNavigation,
-}: {
-  basePath: string
-  section: AbbrevApiReferenceSection
-  realNavigation?: boolean
-}) {
+function RefCategory({ basePath, section, realNavigation }: RefCategoryProps) {
   if (!('items' in section && section.items && section.items.length > 0)) return null
 
   return (
-    <>
-      <Divider />
-      {'title' in section && <SideMenuTitle className="py-2">{section.title}</SideMenuTitle>}
-      <ul className="space-y-2">
+    <div className="pt-2">
+      {'title' in section ? (
+        <span className="block py-1 text-sm font-medium text-foreground-light">
+          {section.title}
+        </span>
+      ) : null}
+      <ul className="mt-1 ml-px border-l pl-3">
         {section.items?.map((item) => (
-          <li key={item.id} className={topLvlRefNavItemStyles}>
-            <RefLink basePath={basePath} section={item} realNavigation={realNavigation} />
+          <li key={item.id}>
+            <RefLink
+              basePath={basePath}
+              section={item}
+              className={ACTIVE_BAR_CLASS_NAME}
+              realNavigation={realNavigation}
+            />
           </li>
         ))}
       </ul>
-    </>
-  )
-}
-
-function Divider() {
-  return <hr className="w-full h-px my-3 bg-control" />
-}
-
-function SideMenuTitle({ children, className }: PropsWithChildren<{ className?: string }>) {
-  return (
-    <div
-      className={cn(
-        'font-mono font-medium text-xs text-foreground tracking-wider uppercase',
-        className
-      )}
-    >
-      {children}
     </div>
   )
 }
diff --git a/apps/docs/features/docs/Reference.sdkPage.tsx b/apps/docs/features/docs/Reference.sdkPage.tsx
index 9f03d453bde..cc7f01aae31 100644
--- a/apps/docs/features/docs/Reference.sdkPage.tsx
+++ b/apps/docs/features/docs/Reference.sdkPage.tsx
@@ -20,6 +20,15 @@ export async function ClientSdkReferencePage({ sdkId, libVersion }: ClientSdkRef
 
   const menuData = NavItems[libraryMeta.meta[libVersion].libId]
 
+  const navigationProps = {
+    libraryId: sdkId,
+    name: menuData.title,
+    menuData: menuData,
+    libPath: libraryMeta.libPath,
+    version: libVersion,
+    isLatestVersion: isLatestVersion,
+  }
+
   return (
     <ReferenceContentScrollHandler
       libPath={libraryMeta.libPath}
@@ -28,16 +37,8 @@ export async function ClientSdkReferencePage({ sdkId, libVersion }: ClientSdkRef
     >
       <SidebarSkeleton
         menuId={libraryMeta.meta[libVersion].libId}
-        NavigationMenu={
-          <ReferenceNavigation
-            libraryId={sdkId}
-            name={menuData.title}
-            menuData={menuData}
-            libPath={libraryMeta.libPath}
-            version={libVersion}
-            isLatestVersion={isLatestVersion}
-          />
-        }
+        NavigationMenu={<ReferenceNavigation {...navigationProps} />}
+        rightRail={<ReferenceNavigation {...navigationProps} hasActiveCrumb />}
       >
         <LayoutMainContent>
           {!isLatestVersion && (
diff --git a/apps/docs/features/docs/Reference.selfHostingPage.tsx b/apps/docs/features/docs/Reference.selfHostingPage.tsx
index 53773af3514..e2054b1d119 100644
--- a/apps/docs/features/docs/Reference.selfHostingPage.tsx
+++ b/apps/docs/features/docs/Reference.selfHostingPage.tsx
@@ -47,20 +47,21 @@ export async function SelfHostingReferencePage({
 
   const name = REFERENCES[servicePath.replaceAll('-', '_')].name
 
+  const navigationProps = {
+    libraryId: servicePath,
+    name: name,
+    menuData: menuData,
+    libPath: servicePath,
+    version: 'latest',
+    isLatestVersion: true,
+  }
+
   return (
     <ReferenceContentScrollHandler libPath={servicePath} version="latest" isLatestVersion={true}>
       <SidebarSkeleton
         menuId={menuId}
-        NavigationMenu={
-          <ReferenceNavigation
-            libraryId={servicePath}
-            name={name}
-            menuData={menuData}
-            libPath={servicePath}
-            version="latest"
-            isLatestVersion={true}
-          />
-        }
+        NavigationMenu={<ReferenceNavigation {...navigationProps} />}
+        rightRail={<ReferenceNavigation {...navigationProps} hasActiveCrumb />}
       >
         <LayoutMainContent>
           <article className="@container/article">