diff --git a/apps/docs/app/reference/[...slug]/page.tsx b/apps/docs/app/reference/[...slug]/page.tsx
index 0ed5497704c..d5b295ac022 100644
--- a/apps/docs/app/reference/[...slug]/page.tsx
+++ b/apps/docs/app/reference/[...slug]/page.tsx
@@ -1,5 +1,3 @@
-import { notFound } from 'next/navigation'
-
 import { REFERENCES } from '~/content/navigation.references'
 import { ApiReferencePage } from '~/features/docs/Reference.apiPage'
 import { CliReferencePage } from '~/features/docs/Reference.cliPage'
@@ -11,6 +9,7 @@ import {
   parseReferencePath,
   redirectNonexistentReferenceSection,
 } from '~/features/docs/Reference.utils'
+import { notFound } from 'next/navigation'
 
 export const dynamicParams = false
 
@@ -46,7 +45,7 @@ export default async function ReferencePage(props: { params: Promise<{ slug: Arr
   } else if (isCliReference) {
     return <CliReferencePage />
   } else if (isApiReference) {
-    return <ApiReferencePage />
+    return <ApiReferencePage sectionSlug={parsedPath.path[0]} />
   } else if (isSelfHostingReference) {
     return (
       <SelfHostingReferencePage service={parsedPath.service} servicePath={parsedPath.servicePath} />
diff --git a/apps/docs/features/docs/Reference.apiPage.tsx b/apps/docs/features/docs/Reference.apiPage.tsx
index 3e77558f3e6..94f2e69e27c 100644
--- a/apps/docs/features/docs/Reference.apiPage.tsx
+++ b/apps/docs/features/docs/Reference.apiPage.tsx
@@ -3,11 +3,13 @@ import { reference_api } from '~/components/Navigation/NavigationMenu/Navigation
 import { ClientLibIntroduction } from '~/features/docs/Reference.introduction'
 import { ReferenceNavigation } from '~/features/docs/Reference.navigation'
 import { ReferenceContentScrollHandler } from '~/features/docs/Reference.navigation.client'
-import { RefSections } from '~/features/docs/Reference.sections'
+import { RefSection } from '~/features/docs/Reference.sections'
 import { LayoutMainContent } from '~/layouts/DefaultLayout'
 import { SidebarSkeleton } from '~/layouts/MainSkeleton'
 
-export async function ApiReferencePage() {
+export async function ApiReferencePage({ sectionSlug }: { sectionSlug?: string }) {
+  const isIndexOrIntro = !sectionSlug || sectionSlug === 'introduction'
+
   return (
     <ReferenceContentScrollHandler libPath="api" version="latest" isLatestVersion={true}>
       <SidebarSkeleton
@@ -20,18 +22,22 @@ export async function ApiReferencePage() {
             libPath="api"
             version="latest"
             isLatestVersion={true}
+            realNavigation
           />
         }
       >
         <LayoutMainContent>
           <article className="@container/article">
-            <ClientLibIntroduction
-              libPath="api"
-              version="latest"
-              isLatestVersion={true}
-              className="max-w-[unset]"
-            />
-            <RefSections libraryId="api" version="latest" />
+            {isIndexOrIntro ? (
+              <ClientLibIntroduction
+                libPath="api"
+                version="latest"
+                isLatestVersion={true}
+                className="max-w-[unset]"
+              />
+            ) : (
+              <RefSection libraryId="api" version="latest" slug={sectionSlug} />
+            )}
           </article>
         </LayoutMainContent>
       </SidebarSkeleton>
diff --git a/apps/docs/features/docs/Reference.navigation.client.tsx b/apps/docs/features/docs/Reference.navigation.client.tsx
index 4ddf294fd20..0211b33f8fd 100644
--- a/apps/docs/features/docs/Reference.navigation.client.tsx
+++ b/apps/docs/features/docs/Reference.navigation.client.tsx
@@ -239,11 +239,13 @@ export function RefLink({
   section,
   skipChildren = false,
   className,
+  realNavigation,
 }: {
   basePath: string
   section: AbbrevApiReferenceSection
   skipChildren?: boolean
   className?: string
+  realNavigation?: boolean
 }) {
   const ref = useRef<HTMLAnchorElement>(null)
 
@@ -272,16 +274,19 @@ export function RefLink({
   return (
     <>
       {isCompoundSection ? (
-        <CompoundRefLink basePath={basePath} section={section} />
+        <CompoundRefLink basePath={basePath} section={section} realNavigation={realNavigation} />
       ) : (
         <Link
           ref={ref}
-          // We don't use these links because we never do real navigation, so
-          // prefetching just wastes egress
-          prefetch={false}
+          // Most reference "pages" are actually an agglomeration of many
+          // "pages", so by default we never do a real navigation and
+          // prefetching would just waste egress. Reference types that render
+          // one real page per section set `realNavigation` and genuinely
+          // benefit from prefetch instead.
+          prefetch={realNavigation ? undefined : false}
           href={href}
           className={getLinkStyles(isActive, className)}
-          onClick={onClick}
+          onClick={realNavigation ? undefined : onClick}
         >
           {section.title}
         </Link>
@@ -321,9 +326,11 @@ function useCompoundRefLinkActive(basePath: string, section: AbbrevApiReferenceS
 function CompoundRefLink({
   basePath,
   section,
+  realNavigation,
 }: {
   basePath: string
   section: AbbrevApiReferenceSection
+  realNavigation?: boolean
 }) {
   const { open, setOpen, isActive } = useCompoundRefLinkActive(basePath, section)
 
@@ -357,7 +364,7 @@ function CompoundRefLink({
           {(section.items || []).map((item, idx) => {
             return (
               <li key={`${section.id}-${idx}`}>
-                <RefLink basePath={basePath} section={item} />
+                <RefLink basePath={basePath} section={item} realNavigation={realNavigation} />
               </li>
             )
           })}
diff --git a/apps/docs/features/docs/Reference.navigation.tsx b/apps/docs/features/docs/Reference.navigation.tsx
index 51e594b2874..5e9b27471e3 100644
--- a/apps/docs/features/docs/Reference.navigation.tsx
+++ b/apps/docs/features/docs/Reference.navigation.tsx
@@ -1,16 +1,14 @@
-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,
   ReferenceNavigationScrollHandler,
+  RefLink,
 } from '~/features/docs/Reference.navigation.client'
 import { type AbbrevApiReferenceSection } from '~/features/docs/Reference.utils'
+import { isFeatureEnabled } from 'common'
+import { type PropsWithChildren } from 'react'
+import { cn } from 'ui'
 
 interface ReferenceNavigationProps {
   libraryId: string
@@ -19,6 +17,7 @@ interface ReferenceNavigationProps {
   libPath: string
   version: string
   isLatestVersion: boolean
+  realNavigation?: boolean
 }
 
 export async function ReferenceNavigation({
@@ -28,6 +27,7 @@ export async function ReferenceNavigation({
   libPath,
   version,
   isLatestVersion,
+  realNavigation,
 }: ReferenceNavigationProps) {
   const navSections = await getReferenceSections(libraryId, version)
   const filteredNavSections = navSections?.filter((section) => section.title !== 'Auth')
@@ -46,11 +46,11 @@ export async function ReferenceNavigation({
         {displayedNavSections?.map((section, index) =>
           section.type === 'category' ? (
             <li key={section.id ?? String(index)}>
-              <RefCategory basePath={basePath} section={section} />
+              <RefCategory basePath={basePath} section={section} realNavigation={realNavigation} />
             </li>
           ) : (
             <li key={section.id ?? String(index)} className={topLvlRefNavItemStyles}>
-              <RefLink basePath={basePath} section={section} />
+              <RefLink basePath={basePath} section={section} realNavigation={realNavigation} />
             </li>
           )
         )}
@@ -64,9 +64,11 @@ const topLvlRefNavItemStyles = 'leading-5'
 function RefCategory({
   basePath,
   section,
+  realNavigation,
 }: {
   basePath: string
   section: AbbrevApiReferenceSection
+  realNavigation?: boolean
 }) {
   if (!('items' in section && section.items && section.items.length > 0)) return null
 
@@ -77,7 +79,7 @@ function RefCategory({
       <ul className="space-y-2">
         {section.items?.map((item) => (
           <li key={item.id} className={topLvlRefNavItemStyles}>
-            <RefLink basePath={basePath} section={item} />
+            <RefLink basePath={basePath} section={item} realNavigation={realNavigation} />
           </li>
         ))}
       </ul>
diff --git a/apps/docs/features/docs/Reference.sections.tsx b/apps/docs/features/docs/Reference.sections.tsx
index cbced0f844c..226ff263ec2 100644
--- a/apps/docs/features/docs/Reference.sections.tsx
+++ b/apps/docs/features/docs/Reference.sections.tsx
@@ -5,6 +5,7 @@ import {
   getCliSpec,
   getFlattenedSections,
   getFunctionsList,
+  getSectionsBySlug,
   getSelfHostedApiEndpointById,
   getTypeSpec,
 } from '~/features/docs/Reference.generated.singleton'
@@ -24,6 +25,7 @@ import type { AbbrevApiReferenceSection } from '~/features/docs/Reference.utils'
 import { normalizeMarkdown } from '~/features/docs/Reference.utils'
 import { CodeBlock } from '~/features/ui/CodeBlock/CodeBlock'
 import { isFeatureEnabled } from 'common'
+import { notFound } from 'next/navigation'
 import { Fragment } from 'react'
 import ReactMarkdown from 'react-markdown'
 import { Badge, cn, Tabs, TabsContent, TabsList, TabsTrigger } from 'ui'
@@ -64,6 +66,24 @@ async function RefSections({ libraryId, version }: RefSectionsProps) {
   )
 }
 
+type RefSectionProps = {
+  libraryId: string
+  version: string
+  slug: string
+}
+
+async function RefSection({ libraryId, version, slug }: RefSectionProps) {
+  const sectionsBySlug = await getSectionsBySlug(libraryId, version)
+  const section = sectionsBySlug?.get(slug)
+  if (!section) notFound()
+
+  return (
+    <div className="flex flex-col my-16 gap-16">
+      <SectionSwitch libraryId={libraryId} version={version} section={section} />
+    </div>
+  )
+}
+
 function trimIntro(sections: Array<AbbrevApiReferenceSection>) {
   const hasIntro = sections[0]?.type === 'markdown' && sections[0]?.slug === 'introduction'
   if (hasIntro) {
@@ -573,4 +593,4 @@ async function FunctionSection({
   )
 }
 
-export { RefSections }
+export { RefSections, RefSection }
diff --git a/apps/docs/features/docs/Reference.utils.ts b/apps/docs/features/docs/Reference.utils.ts
index 5824f27901a..f3680553bbc 100644
--- a/apps/docs/features/docs/Reference.utils.ts
+++ b/apps/docs/features/docs/Reference.utils.ts
@@ -1,5 +1,8 @@
 import { clientSdkIds, REFERENCES, selfHostingServices } from '~/content/navigation.references'
-import { getFlattenedSections } from '~/features/docs/Reference.generated.singleton'
+import {
+  getFlattenedSections,
+  getSectionsBySlug,
+} from '~/features/docs/Reference.generated.singleton'
 import { generateOpenGraphImageMeta } from '~/features/seo/openGraph'
 import { BASE_PATH } from '~/lib/constants'
 import { getCustomContent } from '~/lib/custom-content/getCustomContent'
@@ -113,11 +116,11 @@ export async function generateReferenceStaticParams() {
     },
   ]
 
-  const apiPages = [
-    {
-      slug: ['api'],
-    },
-  ]
+  const apiFlattenedSections = await getFlattenedSections('api', 'latest')
+  const apiPages = (apiFlattenedSections ?? [])
+    .filter((section) => section.type !== 'category' && !!section.slug)
+    .map((section) => ({ slug: ['api', section.slug] }))
+    .concat([{ slug: ['api'] }])
 
   const selfHostingPages = selfHostingServices.map((service) => ({
     slug: [REFERENCES[service].libPath],
@@ -178,9 +181,19 @@ export async function generateReferenceMetadata(
       description: 'CLI reference for the Supabase CLI',
     }
   } else if (isApiReference) {
+    const { path } = parsedPath
+    const sectionSlug = path[0] !== 'introduction' ? path[0] : undefined
+
+    const sectionsBySlug = await getSectionsBySlug('api', 'latest')
+    const sectionTitle = sectionSlug ? sectionsBySlug?.get(sectionSlug)?.title : undefined
+    const url = [BASE_PATH, 'reference', 'api', sectionSlug].filter(Boolean).join('/')
+
     return {
-      title: 'Management API Reference | Supabase Docs',
+      title: `Management API Reference${sectionTitle ? `: ${sectionTitle}` : ''} | Supabase Docs`,
       description: 'Management API reference for the Supabase API',
+      alternates: {
+        canonical: url,
+      },
     }
   } else if (isSelfHostingReference) {
     return {
diff --git a/apps/docs/internals/files/reference-lib.ts b/apps/docs/internals/files/reference-lib.ts
index f1dbafbf5cc..c624d66c04b 100644
--- a/apps/docs/internals/files/reference-lib.ts
+++ b/apps/docs/internals/files/reference-lib.ts
@@ -29,12 +29,14 @@ export async function generateReferencePages() {
         .map(async ({ sdkId, version, libPath, isLatestVersion }) => {
           const flattenedSections = await getFlattenedSections(sdkId, version)
           return (
-            flattenedSections?.map((section) => ({
-              link: isLatestVersion
-                ? `reference/${libPath}/${section.slug}`
-                : `reference/${libPath}/${version}/${section.slug}`,
-              priority: 0.8,
-            })) ?? []
+            flattenedSections
+              ?.filter((section) => !!section.slug)
+              .map((section) => ({
+                link: isLatestVersion
+                  ? `reference/${libPath}/${section.slug}`
+                  : `reference/${libPath}/${version}/${section.slug}`,
+                priority: 0.8,
+              })) ?? []
           )
         })
     )
diff --git a/apps/docs/middleware.test.ts b/apps/docs/middleware.test.ts
index 87d171621d9..509579e088a 100644
--- a/apps/docs/middleware.test.ts
+++ b/apps/docs/middleware.test.ts
@@ -163,3 +163,34 @@ describe('docs middleware — /guides/* content negotiation', () => {
     expect(rewrite).not.toContain('/api/guides-md/')
   })
 })
+
+describe('docs middleware — /reference/api/* routing', () => {
+  // Regression test for INC-703: /reference/api/* used to be collapsed to a
+  // single /reference/api page for every endpoint, which grew unboundedly
+  // with the OpenAPI spec until it exceeded Vercel's ISR page-size cap. Each
+  // endpoint now gets its own statically-generated page, so these paths must
+  // pass through untouched.
+  it('does not rewrite /reference/api/<endpoint-slug> to the bare index', () => {
+    const req = makeRequest('/docs/reference/api/v1-list-all-projects')
+    expect(middleware(req).headers.get(REWRITE_HEADER)).toBeNull()
+  })
+
+  it('does not rewrite the bare /reference/api index', () => {
+    const req = makeRequest('/docs/reference/api')
+    expect(middleware(req).headers.get(REWRITE_HEADER)).toBeNull()
+  })
+
+  it('still rewrites /reference/cli/* to the single CLI page', () => {
+    const req = makeRequest('/docs/reference/cli/some-command')
+    expect(middleware(req).headers.get(REWRITE_HEADER)).toBe(
+      'https://supabase.com/docs/reference/cli'
+    )
+  })
+
+  it('still rewrites /reference/self-hosting-<service>/* to its single service page', () => {
+    const req = makeRequest('/docs/reference/self-hosting-auth/some-endpoint')
+    expect(middleware(req).headers.get(REWRITE_HEADER)).toBe(
+      'https://supabase.com/docs/reference/self-hosting-auth'
+    )
+  })
+})
diff --git a/apps/docs/middleware.ts b/apps/docs/middleware.ts
index fd885725c23..b9bbd611888 100644
--- a/apps/docs/middleware.ts
+++ b/apps/docs/middleware.ts
@@ -63,11 +63,6 @@ export function middleware(request: NextRequest) {
     return NextResponse.rewrite(new URL(rewritePath, request.url))
   }
 
-  if (lib === 'api') {
-    const rewritePath = [REFERENCE_PATH, 'api'].join('/')
-    return NextResponse.rewrite(new URL(rewritePath, request.url))
-  }
-
   if (lib?.startsWith('self-hosting-')) {
     const rewritePath = [REFERENCE_PATH, lib].join('/')
     return NextResponse.rewrite(new URL(rewritePath, request.url))