diff --git a/.changeset/stale-wolves-follow.md b/.changeset/stale-wolves-follow.md
new file mode 100644
index 0000000000..791e5e3710
--- /dev/null
+++ b/.changeset/stale-wolves-follow.md
@@ -0,0 +1,5 @@
+---
+'@shopify/app': minor
+---
+
+Enable custom headers in CLI GraphiQL. Users can now set custom headers like `Shopify-Search-Query-Debug=1` in the GraphiQL interface to pass debugging headers to the Admin API.
diff --git a/packages/app/src/cli/services/dev/graphiql/server.ts b/packages/app/src/cli/services/dev/graphiql/server.ts
index 30bda113e6..266d62c834 100644
--- a/packages/app/src/cli/services/dev/graphiql/server.ts
+++ b/packages/app/src/cli/services/dev/graphiql/server.ts
@@ -1,5 +1,6 @@
 import {defaultQuery, graphiqlTemplate} from './templates/graphiql.js'
 import {unauthorizedTemplate} from './templates/unauthorized.js'
+import {filterCustomHeaders} from './utilities.js'
 import express from 'express'
 import bodyParser from 'body-parser'
 import {performActionWithRetryAfterRecovery} from '@shopify/cli-kit/common/retry'
@@ -185,8 +186,12 @@ export function setupGraphiQLServer({
     try {
       const reqBody = JSON.stringify(req.body)
 
+      // Extract custom headers from the request, filtering out blocked headers
+      const customHeaders = filterCustomHeaders(req.headers)
+
       const runRequest = async () => {
         const headers = {
+          ...customHeaders,
           Accept: 'application/json',
           'Content-Type': 'application/json',
           'X-Shopify-Access-Token': await token(),
diff --git a/packages/app/src/cli/services/dev/graphiql/templates/graphiql.tsx b/packages/app/src/cli/services/dev/graphiql/templates/graphiql.tsx
index a767c70743..1379e7d3a7 100644
--- a/packages/app/src/cli/services/dev/graphiql/templates/graphiql.tsx
+++ b/packages/app/src/cli/services/dev/graphiql/templates/graphiql.tsx
@@ -265,7 +265,7 @@ export function graphiqlTemplate({
                 {query: "{%if query.preface %}{{query.preface}}\\n{% endif %}{{query.query}}", variables: "{{query.variables}}"},
               {%endfor%}
             ],
-            isHeadersEditorEnabled: false,
+            isHeadersEditorEnabled: true,
           }),
           document.getElementById('graphiql-explorer'),
         )
diff --git a/packages/app/src/cli/services/dev/graphiql/utilities.test.ts b/packages/app/src/cli/services/dev/graphiql/utilities.test.ts
new file mode 100644
index 0000000000..473260fd05
--- /dev/null
+++ b/packages/app/src/cli/services/dev/graphiql/utilities.test.ts
@@ -0,0 +1,99 @@
+import {filterCustomHeaders} from './utilities.js'
+import {describe, expect, test} from 'vitest'
+
+describe('filterCustomHeaders', () => {
+  test('allows custom headers that are not blocked', () => {
+    const headers = {
+      'x-custom-header': 'custom-value',
+      'x-another-header': 'another-value',
+    }
+
+    const result = filterCustomHeaders(headers)
+
+    expect(result).toEqual({
+      'x-custom-header': 'custom-value',
+      'x-another-header': 'another-value',
+    })
+  })
+
+  test('blocks hop-by-hop headers', () => {
+    const headers = {
+      connection: 'keep-alive',
+      'keep-alive': 'timeout=5',
+      'transfer-encoding': 'chunked',
+      'x-custom-header': 'custom-value',
+    }
+
+    const result = filterCustomHeaders(headers)
+
+    expect(result).toEqual({
+      'x-custom-header': 'custom-value',
+    })
+  })
+
+  test('blocks proxy-controlled headers', () => {
+    const headers = {
+      host: 'localhost:3000',
+      'content-type': 'application/json',
+      accept: 'application/json',
+      'user-agent': 'Mozilla/5.0',
+      authorization: 'Bearer token',
+      cookie: 'session=abc',
+      'x-shopify-access-token': 'secret-token',
+      'x-custom-header': 'custom-value',
+    }
+
+    const result = filterCustomHeaders(headers)
+
+    expect(result).toEqual({
+      'x-custom-header': 'custom-value',
+    })
+  })
+
+  test('blocks headers case-insensitively', () => {
+    const headers = {
+      Connection: 'keep-alive',
+      HOST: 'localhost',
+      'Content-Type': 'application/json',
+      'X-Custom-Header': 'custom-value',
+    }
+
+    const result = filterCustomHeaders(headers)
+
+    expect(result).toEqual({
+      'X-Custom-Header': 'custom-value',
+    })
+  })
+
+  test('filters out non-string header values', () => {
+    const headers: {[key: string]: string | string[] | undefined} = {
+      'x-custom-header': 'custom-value',
+      'x-array-header': ['value1', 'value2'],
+      'x-undefined-header': undefined,
+    }
+
+    const result = filterCustomHeaders(headers)
+
+    expect(result).toEqual({
+      'x-custom-header': 'custom-value',
+    })
+  })
+
+  test('returns empty object when all headers are blocked', () => {
+    const headers = {
+      host: 'localhost',
+      connection: 'keep-alive',
+      'content-type': 'application/json',
+    }
+
+    const result = filterCustomHeaders(headers)
+
+    expect(result).toEqual({})
+  })
+
+  test('returns empty object for empty input', () => {
+    const result = filterCustomHeaders({})
+
+    expect(result).toEqual({})
+  })
+})
diff --git a/packages/app/src/cli/services/dev/graphiql/utilities.ts b/packages/app/src/cli/services/dev/graphiql/utilities.ts
new file mode 100644
index 0000000000..d900e44309
--- /dev/null
+++ b/packages/app/src/cli/services/dev/graphiql/utilities.ts
@@ -0,0 +1,42 @@
+/**
+ * Headers that should NOT be forwarded from the GraphiQL client to the Admin API.
+ * These include:
+ * - Hop-by-hop headers (RFC 7230) that are connection-specific
+ * - Browser-specific headers that are not relevant to API requests
+ * - Headers the proxy sets itself (auth, content-type, etc.)
+ */
+const BLOCKED_HEADERS = new Set([
+  // Hop-by-hop headers (RFC 7230 Section 6.1)
+  'connection',
+  'keep-alive',
+  'proxy-authenticate',
+  'proxy-authorization',
+  'te',
+  'trailer',
+  'transfer-encoding',
+  'upgrade',
+
+  // Headers the proxy controls
+  'host',
+  'content-length',
+  'content-type',
+  'accept',
+  'user-agent',
+  'authorization',
+  'cookie',
+  'x-shopify-access-token',
+])
+
+/**
+ * Filters request headers to extract only custom headers that are safe to forward.
+ * Blocked headers and non-string values are excluded.
+ */
+export function filterCustomHeaders(headers: {[key: string]: string | string[] | undefined}): {[key: string]: string} {
+  const customHeaders: {[key: string]: string} = {}
+  for (const [key, value] of Object.entries(headers)) {
+    if (!BLOCKED_HEADERS.has(key.toLowerCase()) && typeof value === 'string') {
+      customHeaders[key] = value
+    }
+  }
+  return customHeaders
+}