diff --git a/src/app/(space)/fetch.ts b/src/app/(space)/fetch.ts
index c73b5ac03..7e7203308 100644
--- a/src/app/(space)/fetch.ts
+++ b/src/app/(space)/fetch.ts
@@ -40,6 +40,7 @@ export function getContentPointer(): ContentPointer | SiteContentPointer {
     if (siteId) {
         const organizationId = headerSet.get('x-gitbook-content-organization');
         const siteSpaceId = headerSet.get('x-gitbook-content-site-space');
+        const siteUrl = headerSet.get('x-gitbook-content-url');
         if (!organizationId) {
             throw new Error('Missing site content headers');
         }
@@ -48,6 +49,7 @@ export function getContentPointer(): ContentPointer | SiteContentPointer {
             siteId,
             spaceId,
             siteSpaceId: siteSpaceId ?? undefined,
+            siteUrl: siteUrl ?? undefined,
             organizationId,
             revisionId: headerSet.get('x-gitbook-content-revision') ?? undefined,
             changeRequestId: headerSet.get('x-gitbook-content-changerequest') ?? undefined,
@@ -71,7 +73,10 @@ export async function fetchSpaceData() {
 
     const [{ space, contentTarget, pages, customization, scripts }, parentSite] = await Promise.all(
         'siteId' in content
-            ? [getCurrentSiteData(content), fetchParentSite(content.organizationId, content.siteId)]
+            ? [
+                  getCurrentSiteData(content),
+                  fetchParentSite(content.organizationId, content.siteId, content.siteUrl),
+              ]
             : [getSpaceData(content)],
     );
 
@@ -102,7 +107,7 @@ export async function fetchPageData(params: PagePathParams | PageIdParams) {
     const page = await resolvePage(contentTarget, pages, params);
     const [parent, document] = await Promise.all([
         'siteId' in content
-            ? fetchParentSite(content.organizationId, content.siteId)
+            ? fetchParentSite(content.organizationId, content.siteId, content.siteUrl)
             : fetchParentCollection(space),
         page?.page.documentId ? getDocument(space.id, page.page.documentId) : null,
     ]);
@@ -173,10 +178,14 @@ async function fetchParentCollection(space: Space) {
     return { parent: collection, spaces };
 }
 
-async function fetchParentSite(organizationId: string, siteId: string) {
+async function fetchParentSite(
+    organizationId: string,
+    siteId: string,
+    siteUrl: string | undefined,
+) {
     const [site, siteSpaces] = await Promise.all([
         getSite(organizationId, siteId),
-        getSiteSpaces(organizationId, siteId),
+        getSiteSpaces(organizationId, siteId, siteUrl ?? null),
     ]);
 
     const spaces: Record<string, Space> = {};
diff --git a/src/components/Search/server-actions.tsx b/src/components/Search/server-actions.tsx
index cbd0395b5..743cb2bff 100644
--- a/src/components/Search/server-actions.tsx
+++ b/src/components/Search/server-actions.tsx
@@ -76,7 +76,7 @@ export async function searchParentContent(
         api.searchParentContent(parent.id, query),
         parent.object === 'collection' ? api.getCollectionSpaces(parent.id) : null,
         parent.object === 'site' && 'organizationId' in pointer
-            ? api.getSiteSpaces(pointer.organizationId, parent.id)
+            ? api.getSiteSpaces(pointer.organizationId, parent.id, pointer.siteUrl ?? null)
             : null,
     ]);
 
diff --git a/src/lib/api.ts b/src/lib/api.ts
index 1da689af9..f6c1b9f64 100644
--- a/src/lib/api.ts
+++ b/src/lib/api.ts
@@ -47,6 +47,11 @@ export interface SiteContentPointer extends ContentPointer {
      * ID of the siteSpace can be undefined when rendering in multi-id mode (for site previews)
      */
     siteSpaceId: string | undefined;
+    /**
+     * URL of the site content that was used for lookup. Only set for `multi` and `multi-path` modes
+     * where an URL is involved in the lookup/resolution
+     */
+    siteUrl: string | undefined;
 }
 
 /**
@@ -126,6 +131,8 @@ export type PublishedContentWithCache =
     | ((PublishedContentLookup | PublishedSiteContentLookup) & {
           cacheMaxAge?: number;
           cacheTags?: string[];
+          /** Published content URL that was used for lookup */
+          contentUrl?: string;
       })
     | {
           error: {
@@ -235,6 +242,7 @@ export const getPublishedContentByUrl = cache(
                 ...response.data,
                 cacheMaxAge: parsed.ttl,
                 cacheTags: parsed.tags,
+                contentUrl: url,
             };
             return {
                 tags: [
@@ -736,12 +744,28 @@ export const getSite = cache(
  */
 export const getSiteSpaces = cache(
     'api.getSiteSpaces',
-    async (organizationId: string, siteId: string, options: CacheFunctionOptions) => {
+    async (
+        organizationId: string,
+        siteId: string,
+        /**
+         * Additional site URL that can be used as context to resolve site space published urls
+         */
+        siteUrlContext: string | null,
+        options: CacheFunctionOptions,
+    ) => {
         const response = await getAll((params) =>
-            api().orgs.listSiteSpaces(organizationId, siteId, params, {
-                ...noCacheFetchOptions,
-                signal: options.signal,
-            }),
+            api().orgs.listSiteSpaces(
+                organizationId,
+                siteId,
+                {
+                    ...params,
+                    context: siteUrlContext ?? undefined,
+                },
+                {
+                    ...noCacheFetchOptions,
+                    signal: options.signal,
+                },
+            ),
         );
 
         return cacheResponse(response, {
diff --git a/src/middleware.ts b/src/middleware.ts
index fbd262311..bdbad2831 100644
--- a/src/middleware.ts
+++ b/src/middleware.ts
@@ -209,6 +209,9 @@ export async function middleware(request: NextRequest) {
             headers.set('x-gitbook-content-site-space', resolved.siteSpace);
         }
     }
+    if (resolved.contentUrl) {
+        headers.set('x-gitbook-content-url', resolved.contentUrl);
+    }
     if (resolved.revision) {
         headers.set('x-gitbook-content-revision', resolved.revision);
     }
@@ -659,6 +662,7 @@ async function lookupSpaceByAPI(
             apiToken: data.apiToken,
             cacheMaxAge: data.cacheMaxAge,
             cacheTags: data.cacheTags,
+            contentUrl: data.contentUrl,
             ...('site' in data
                 ? { site: data.site, siteSpace: data.siteSpace, organization: data.organization }
                 : {}),