diff --git a/packages/verified-fetch/src/utils/parse-resource.ts b/packages/verified-fetch/src/utils/parse-resource.ts
index a65a1904..ea2045df 100644
--- a/packages/verified-fetch/src/utils/parse-resource.ts
+++ b/packages/verified-fetch/src/utils/parse-resource.ts
@@ -32,6 +32,7 @@ export async function parseResource (resource: Resource, { ipns, logger }: Parse
       protocol: 'ipfs',
       path: '',
       query: {},
+      ipfsPath: `/ipfs/${cid.toString()}`,
       ttl: 29030400 // 1 year for ipfs content
     } satisfies ParsedUrlStringResults
   }
diff --git a/packages/verified-fetch/src/utils/parse-url-string.ts b/packages/verified-fetch/src/utils/parse-url-string.ts
index 63959365..ef39bb4f 100644
--- a/packages/verified-fetch/src/utils/parse-url-string.ts
+++ b/packages/verified-fetch/src/utils/parse-url-string.ts
@@ -27,6 +27,16 @@ interface ParsedUrlStringResultsBase extends ResolveResult {
   protocol: 'ipfs' | 'ipns'
   query: ParsedUrlQuery
 
+  /**
+   * The value for the IPFS gateway spec compliant header `X-Ipfs-Path` on the
+   * response.
+   * The value of this header should be the original requested content path,
+   * prior to any path resolution or traversal.
+   *
+   * @see https://specs.ipfs.tech/http-gateways/path-gateway/#x-ipfs-path-response-header
+   */
+  ipfsPath: string
+
   /**
    * seconds as a number
    */
@@ -248,7 +258,8 @@ export async function parseUrlString ({ urlString, ipns, logger }: ParseUrlStrin
     cid,
     path: joinPaths(resolvedPath, urlPath ?? ''),
     query,
-    ttl
+    ttl,
+    ipfsPath: `/${protocol}/${cidOrPeerIdOrDnsLink}${urlPath != null && urlPath !== '' ? `/${urlPath}` : ''}`
   } satisfies ParsedUrlStringResults
 }
 
diff --git a/packages/verified-fetch/src/verified-fetch.ts b/packages/verified-fetch/src/verified-fetch.ts
index 83231062..0a1d9cb9 100644
--- a/packages/verified-fetch/src/verified-fetch.ts
+++ b/packages/verified-fetch/src/verified-fetch.ts
@@ -490,6 +490,7 @@ export class VerifiedFetch {
     let query: ParsedUrlStringResults['query']
     let ttl: ParsedUrlStringResults['ttl']
     let protocol: ParsedUrlStringResults['protocol']
+    let ipfsPath: string
     try {
       const result = await parseResource(resource, { ipns: this.ipns, logger: this.helia.logger }, options)
       cid = result.cid
@@ -497,6 +498,7 @@ export class VerifiedFetch {
       query = result.query
       ttl = result.ttl
       protocol = result.protocol
+      ipfsPath = result.ipfsPath
     } catch (err: any) {
       options?.signal?.throwIfAborted()
       this.log.error('error parsing resource %s', resource, err)
@@ -558,8 +560,7 @@ export class VerifiedFetch {
     response.headers.set('etag', getETag({ cid, reqFormat, weak: false }))
 
     setCacheControlHeader({ response, ttl, protocol })
-    // https://specs.ipfs.tech/http-gateways/path-gateway/#x-ipfs-path-response-header
-    response.headers.set('X-Ipfs-Path', resource.toString())
+    response.headers.set('X-Ipfs-Path', ipfsPath)
 
     // set Content-Disposition header
     let contentDisposition: string | undefined
diff --git a/packages/verified-fetch/test/parse-resource.spec.ts b/packages/verified-fetch/test/parse-resource.spec.ts
index 05a30192..e903a0aa 100644
--- a/packages/verified-fetch/test/parse-resource.spec.ts
+++ b/packages/verified-fetch/test/parse-resource.spec.ts
@@ -1,17 +1,20 @@
 import { defaultLogger } from '@libp2p/logger'
+import { createEd25519PeerId } from '@libp2p/peer-id-factory'
 import { expect } from 'aegir/chai'
 import { CID } from 'multiformats/cid'
 import sinon from 'sinon'
-import { stubInterface } from 'sinon-ts'
+import { stubInterface, type StubbedInstance } from 'sinon-ts'
 import { parseResource } from '../src/utils/parse-resource.js'
 import type { IPNS } from '@helia/ipns'
 
+const testCID = CID.parse('QmQJ8fxavY54CUsxMSx9aE9Rdcmvhx8awJK2jzJp4iAqCr')
+const peerId = await createEd25519PeerId()
+
 describe('parseResource', () => {
   it('does not call @helia/ipns for CID', async () => {
-    const testCID = CID.parse('QmQJ8fxavY54CUsxMSx9aE9Rdcmvhx8awJK2jzJp4iAqCr')
     const shouldNotBeCalled1 = sinon.stub().throws(new Error('should not be called'))
     const shouldNotBeCalled2 = sinon.stub().throws(new Error('should not be called'))
-    const { cid, path, query } = await parseResource(testCID, {
+    const { cid, path, query, ipfsPath } = await parseResource(testCID, {
       ipns: stubInterface<IPNS>({
         resolveDNSLink: shouldNotBeCalled1,
         resolve: shouldNotBeCalled2
@@ -23,10 +26,49 @@ describe('parseResource', () => {
     expect(cid.toString()).to.equal(testCID.toString())
     expect(path).to.equal('')
     expect(query).to.deep.equal({})
+    expect(ipfsPath).to.equal(`/ipfs/${testCID.toString()}`)
   })
 
   it('throws an error if given an invalid resource', async () => {
     // @ts-expect-error - purposefully invalid input
     await expect(parseResource({}, stubInterface<IPNS>())).to.be.rejectedWith('Invalid resource.')
   })
+
+  describe('ipfsPath', () => {
+    let ipnsStub: StubbedInstance<IPNS>
+
+    beforeEach(async () => {
+      ipnsStub = stubInterface<IPNS>({
+        resolveDNSLink: sinon.stub().returns({ cid: testCID }),
+        resolve: sinon.stub().returns({ cid: testCID })
+      })
+    });
+
+    [
+      // resource without paths
+      { resource: testCID, expectedValue: `/ipfs/${testCID}` },
+      { resource: `ipfs://${testCID}`, expectedValue: `/ipfs/${testCID}` },
+      { resource: `http://example.com/ipfs/${testCID}`, expectedValue: `/ipfs/${testCID}` },
+      { resource: `ipns://${peerId}`, expectedValue: `/ipns/${peerId}` },
+      { resource: `http://example.com/ipns/${peerId}`, expectedValue: `/ipns/${peerId}` },
+      { resource: 'ipns://specs.ipfs.tech', expectedValue: '/ipns/specs.ipfs.tech' },
+      { resource: 'http://example.com/ipns/specs.ipfs.tech', expectedValue: '/ipns/specs.ipfs.tech' },
+      // resources with paths
+      { resource: `ipfs://${testCID}/foobar`, expectedValue: `/ipfs/${testCID}/foobar` },
+      { resource: `http://example.com/ipfs/${testCID}/foobar`, expectedValue: `/ipfs/${testCID}/foobar` },
+      { resource: `ipns://${peerId}/foobar`, expectedValue: `/ipns/${peerId}/foobar` },
+      { resource: `http://example.com/ipns/${peerId}/foobar`, expectedValue: `/ipns/${peerId}/foobar` },
+      { resource: 'ipns://specs.ipfs.tech/foobar', expectedValue: '/ipns/specs.ipfs.tech/foobar' },
+      { resource: 'http://example.com/ipns/specs.ipfs.tech/foobar', expectedValue: '/ipns/specs.ipfs.tech/foobar' }
+    ].forEach(({ resource, expectedValue }) => {
+      it(`should return the correct ipfsPath for "${resource}"`, async () => {
+        const { ipfsPath } = await parseResource(resource, {
+          ipns: ipnsStub,
+          logger: defaultLogger()
+        })
+
+        expect(ipfsPath).to.equal(expectedValue)
+      })
+    })
+  })
 })
diff --git a/packages/verified-fetch/test/verified-fetch.spec.ts b/packages/verified-fetch/test/verified-fetch.spec.ts
index 9e202749..bb617e3a 100644
--- a/packages/verified-fetch/test/verified-fetch.spec.ts
+++ b/packages/verified-fetch/test/verified-fetch.spec.ts
@@ -157,6 +157,7 @@ describe('@helia/verifed-fetch', () => {
       expect(ipfsResponse).to.be.ok()
       expect(ipfsResponse.status).to.equal(301)
       expect(ipfsResponse.headers.get('location')).to.equal(`ipfs://${res.cid}/foo/`)
+      expect(ipfsResponse.headers.get('X-Ipfs-Path')).to.equal(`/ipfs/${res.cid}/foo`)
       expect(ipfsResponse.url).to.equal(`ipfs://${res.cid}/foo`)
     })