diff --git a/packages/app/src/cli/models/app/loader.test.ts b/packages/app/src/cli/models/app/loader.test.ts
index 23fba409ba..d87c174957 100644
--- a/packages/app/src/cli/models/app/loader.test.ts
+++ b/packages/app/src/cli/models/app/loader.test.ts
@@ -15,7 +15,8 @@ import {ExtensionInstance} from '../extensions/extension-instance.js'
 import {configurationFileNames, blocks} from '../../constants.js'
 import metadata from '../../metadata.js'
 import {loadLocalExtensionsSpecifications} from '../extensions/load-specifications.js'
-import {ExtensionSpecification} from '../extensions/specification.js'
+import {ExtensionSpecification, createContractBasedModuleSpecification} from '../extensions/specification.js'
+import {unifiedConfigurationParserFactory} from '../../utilities/json-schema.js'
 import {getCachedAppInfo} from '../../services/local-storage.js'
 import use from '../../services/app/config/use.js'
 import {WebhooksSchema} from '../extensions/specifications/app_config_webhook_schemas/webhooks_schema.js'
@@ -2666,6 +2667,44 @@ describe('load', () => {
     expect(app).toBeDefined()
     expect(app.name).toBe('for-testing')
   })
+
+  test('does not flag a contract-based configuration spec section as unsupported', async () => {
+    // Given: A TOML config with a section that matches a contract-based config spec
+    const configWithContractSection = buildAppConfiguration({
+      extra: '[purchase_options]\nbundles = true',
+    })
+    await writeConfig(configWithContractSection)
+
+    // Create a contract-based config spec (mimicking a remote-only spec like purchase_options)
+    const contractSpec = createContractBasedModuleSpecification({
+      identifier: 'purchase_options',
+      uidStrategy: 'single',
+      experience: 'configuration',
+      appModuleFeatures: () => [],
+    })
+
+    // Attach a unified parser with the JSON schema contract, like the real flow does
+    const validationSchema = {
+      jsonSchema:
+        '{"type":"object","additionalProperties":false,"properties":{"bundles":{"type":"boolean","description":"Whether the app supports purchase options on bundle products"}}}',
+    }
+    const parseConfigurationObject = await unifiedConfigurationParserFactory(
+      contractSpec as any,
+      validationSchema,
+      'strip',
+    )
+    const specsWithContract = [...specifications, {...contractSpec, parseConfigurationObject}]
+
+    // When: The app is loaded with the contract-based spec included
+    const app = await loadApp({
+      directory: tmpDir,
+      specifications: specsWithContract,
+      userProvidedConfigName: undefined,
+    })
+
+    // Then: No "unsupported section" error for purchase_options
+    expect(app.errors.isEmpty()).toBe(true)
+  })
 })
 
 describe('getAppConfigurationFileName', () => {
diff --git a/packages/app/src/cli/models/app/loader.ts b/packages/app/src/cli/models/app/loader.ts
index 285754067c..0f4ca6c7a8 100644
--- a/packages/app/src/cli/models/app/loader.ts
+++ b/packages/app/src/cli/models/app/loader.ts
@@ -787,8 +787,21 @@ class AppLoader<TConfig extends CurrentAppConfiguration, TModuleSpec extends Ext
             return [null, [] as string[]] as const
           }
           const specConfiguration = specResult.data
+          let claimedKeys = Object.keys(specConfiguration)
+
+          // For contract-based configuration specs (remote-only specs using zod.any()), the
+          // parsed result contains section contents (e.g. {bundles: true}) rather than the
+          // top-level TOML key (e.g. purchase_options). Replace claimedKeys with just the
+          // identifier to avoid falsely claiming unrelated top-level keys that happen to
+          // collide with nested section content keys.
+          if (
+            !claimedKeys.includes(specification.identifier) &&
+            specification.identifier in (appConfiguration as Record<string, unknown>)
+          ) {
+            claimedKeys = [specification.identifier]
+          }
 
-          if (Object.keys(specConfiguration).length === 0) return [null, Object.keys(specConfiguration)] as const
+          if (Object.keys(specConfiguration).length === 0) return [null, claimedKeys] as const
 
           const instance = await this.createExtensionInstance(
             specification.identifier,
@@ -802,7 +815,7 @@ class AppLoader<TConfig extends CurrentAppConfiguration, TModuleSpec extends Ext
               extensionInstance,
             ),
           )
-          return [instance, Object.keys(specConfiguration)] as const
+          return [instance, claimedKeys] as const
         }),
     )
 
diff --git a/packages/app/src/cli/models/extensions/specification.integration.test.ts b/packages/app/src/cli/models/extensions/specification.integration.test.ts
index f49d0712f3..98db6bcd13 100644
--- a/packages/app/src/cli/models/extensions/specification.integration.test.ts
+++ b/packages/app/src/cli/models/extensions/specification.integration.test.ts
@@ -9,6 +9,7 @@ import {BaseSchema} from './schemas.js'
 import {ClientSteps} from '../../services/build/client-steps.js'
 import {AppSchema} from '../app/app.js'
 import {describe, test, expect, beforeAll} from 'vitest'
+import {zod} from '@shopify/cli-kit/node/schema'
 
 // If the AppSchema is not instanced, the dynamic loading of loadLocalExtensionsSpecifications is not working
 beforeAll(() => {
@@ -126,6 +127,63 @@ describe('createConfigExtensionSpecification', () => {
   })
 })
 
+describe('contributeToAppConfigurationSchema', () => {
+  test('contract-based config spec with zod.any() contributes its identifier as a known key', () => {
+    // Given: A contract-based config spec with experience: 'configuration' and zod.any() schema
+    const spec = createContractBasedModuleSpecification({
+      identifier: 'purchase_options',
+      uidStrategy: 'single',
+      experience: 'configuration',
+      appModuleFeatures: () => [],
+    })
+
+    // When: It contributes to the app configuration schema
+    const baseSchema = zod.object({client_id: zod.string()})
+    const result = spec.contributeToAppConfigurationSchema(baseSchema)
+
+    // Then: The resulting schema should accept the identifier as a valid key
+    const parsed = result.safeParse({client_id: 'test', purchase_options: {bundles: true}})
+    expect(parsed.success).toBe(true)
+  })
+
+  test('contract-based config spec with experience: extension does not contribute to schema', () => {
+    // Given: A contract-based spec with experience: 'extension' (not 'configuration')
+    const spec = createContractBasedModuleSpecification({
+      identifier: 'some_extension',
+      uidStrategy: 'uuid',
+      experience: 'extension',
+      appModuleFeatures: () => [],
+    })
+
+    // When: It tries to contribute to the app configuration schema
+    const baseSchema = zod.object({client_id: zod.string()}).strict()
+    const result = spec.contributeToAppConfigurationSchema(baseSchema)
+
+    // Then: The schema should be unchanged — 'some_extension' is not accepted
+    const parsed = result.safeParse({client_id: 'test', some_extension: {enabled: true}})
+    expect(parsed.success).toBe(false)
+  })
+
+  test('config spec with explicit zod schema merges its schema shape', () => {
+    // Given: A locally-defined config spec with an explicit zod schema
+    const spec = createConfigExtensionSpecification({
+      identifier: 'test_config',
+      schema: BaseSchema.extend({
+        my_section: zod.object({enabled: zod.boolean()}).optional(),
+      }),
+      transformConfig: {},
+    })
+
+    // When: It contributes to the app configuration schema
+    const baseSchema = zod.object({client_id: zod.string()})
+    const result = spec.contributeToAppConfigurationSchema(baseSchema)
+
+    // Then: The schema should accept 'my_section' as a valid key
+    const parsed = result.safeParse({client_id: 'test', my_section: {enabled: true}})
+    expect(parsed.success).toBe(true)
+  })
+})
+
 describe('configWithoutFirstClassFields', () => {
   test('removes the first class fields from the config', () => {
     // When
diff --git a/packages/app/src/cli/models/extensions/specification.ts b/packages/app/src/cli/models/extensions/specification.ts
index 457f4408aa..09fe628b1f 100644
--- a/packages/app/src/cli/models/extensions/specification.ts
+++ b/packages/app/src/cli/models/extensions/specification.ts
@@ -226,13 +226,20 @@ export function createExtensionSpecification<TConfiguration extends BaseConfigTy
       // This filters out webhook subscription specifications from contributing to the app configuration schema
       const hasSingleUidStrategy = merged.uidStrategy === 'single'
 
-      const canContribute = isConfig && hasSchema && hasSingleUidStrategy
-      if (!canContribute) {
-        // no change
+      if (!isConfig || !hasSingleUidStrategy) {
         return appConfigSchema
       }
+
+      if (hasSchema) {
+        // eslint-disable-next-line @typescript-eslint/no-explicit-any
+        return (appConfigSchema as any).merge(merged.schema)
+      }
+
+      // For contract-based config specs (e.g. remote-only specs with zod.any()), contribute
+      // the spec identifier as a known top-level key so it isn't flagged as unsupported.
+      const contractSchema = zod.object({[merged.identifier]: zod.any().optional()})
       // eslint-disable-next-line @typescript-eslint/no-explicit-any
-      return (appConfigSchema as any).merge(merged.schema)
+      return (appConfigSchema as any).merge(contractSchema)
     },
     parseConfigurationObject: (configurationObject: unknown) => {
       const parseResult = merged.schema.safeParse(configurationObject)
diff --git a/packages/app/src/cli/utilities/json-schema.test.ts b/packages/app/src/cli/utilities/json-schema.test.ts
index c139dc6e3d..47a0ff1da0 100644
--- a/packages/app/src/cli/utilities/json-schema.test.ts
+++ b/packages/app/src/cli/utilities/json-schema.test.ts
@@ -152,6 +152,85 @@ describe('unifiedConfigurationParserFactory', () => {
     expect(priceError).toBeDefined()
   })
 
+  test('scopes validation to the section contents for configuration specs when identifier matches a key in the config', async () => {
+    // Given: A contract-based config spec (like purchase_options) where the JSON schema
+    // describes the section contents ({bundles: boolean}), and the parser receives the
+    // entire app config with the section nested under the identifier key.
+    const merged = {
+      identifier: 'purchase_options',
+      experience: 'configuration',
+      parseConfigurationObject: mockParseConfigurationObject,
+      validationSchema: {
+        jsonSchema:
+          '{"type":"object","additionalProperties":false,"properties":{"bundles":{"type":"boolean","description":"Whether the app supports purchase options on bundle products"}}}',
+      },
+    }
+
+    // When: The parser receives a full app config where "purchase_options" is a nested section
+    const parser = await unifiedConfigurationParserFactory(merged as any, merged.validationSchema, 'strip')
+    const result = parser({
+      client_id: 'test-id',
+      name: 'my-app',
+      purchase_options: {bundles: true},
+      webhooks: {api_version: '2024-01'},
+    })
+
+    // Then: The parser should scope to the section, validate {bundles: true} against the
+    // schema, and return only the section contents — not an empty object.
+    expect(result.state).toBe('ok')
+    expect(result.data).toEqual({bundles: true})
+  })
+
+  test('returns empty object when config spec identifier is not present in the config', async () => {
+    // Given: Same contract-based config spec, but the TOML doesn't include the section
+    const merged = {
+      identifier: 'purchase_options',
+      experience: 'configuration',
+      parseConfigurationObject: mockParseConfigurationObject,
+      validationSchema: {
+        jsonSchema:
+          '{"type":"object","additionalProperties":false,"properties":{"bundles":{"type":"boolean","description":"Whether the app supports purchase options on bundle products"}}}',
+      },
+    }
+
+    // When: The config does NOT contain "purchase_options"
+    const parser = await unifiedConfigurationParserFactory(merged as any, merged.validationSchema, 'strip')
+    const result = parser({
+      client_id: 'test-id',
+      name: 'my-app',
+      webhooks: {api_version: '2024-01'},
+    })
+
+    // Then: No scoping happens; strip removes all non-matching keys, leaving {}
+    expect(result.state).toBe('ok')
+    expect(result.data).toEqual({})
+  })
+
+  test('validates section contents against the JSON schema when scoped', async () => {
+    // Given: A config spec with a required field in the JSON schema
+    const merged = {
+      identifier: 'my_config',
+      experience: 'configuration',
+      parseConfigurationObject: mockParseConfigurationObject,
+      validationSchema: {
+        jsonSchema:
+          '{"type":"object","additionalProperties":false,"properties":{"enabled":{"type":"boolean"}},"required":["enabled"]}',
+      },
+    }
+
+    // When: The section exists but is missing the required field
+    const parser = await unifiedConfigurationParserFactory(merged as any, merged.validationSchema, 'strip')
+    const result = parser({
+      client_id: 'test-id',
+      my_config: {not_enabled: true},
+    })
+
+    // Then: Validation should fail because "enabled" is required
+    expect(result.state).toBe('error')
+    expect(result.errors).toBeDefined()
+    expect(result.errors!.length).toBeGreaterThan(0)
+  })
+
   test('adds base properties to the JSON schema', async () => {
     // Given
     const merged = {
diff --git a/packages/app/src/cli/utilities/json-schema.ts b/packages/app/src/cli/utilities/json-schema.ts
index 76ac3d5e41..ad779063c2 100644
--- a/packages/app/src/cli/utilities/json-schema.ts
+++ b/packages/app/src/cli/utilities/json-schema.ts
@@ -49,7 +49,18 @@ export async function unifiedConfigurationParserFactory(
 
     // Then, even if this failed, we try to validate against the contract.
     const zodValidatedData = zodParse.state === 'ok' ? zodParse.data : undefined
-    const subjectForAjv = zodValidatedData ?? (config as JsonMapType)
+    let subjectForAjv = zodValidatedData ?? (config as JsonMapType)
+
+    // For contract-based specs (remote-only specs with zod.any()), the zod parse returns the
+    // entire app config. The JSON schema contract describes the section contents (e.g.
+    // {bundles: boolean} for purchase_options), not the whole config. If the spec identifier
+    // exists as a key in the parsed data, scope to that section before validating.
+    if (extensionIdentifier in subjectForAjv) {
+      const sectionData = subjectForAjv[extensionIdentifier as keyof typeof subjectForAjv]
+      if (sectionData !== null && typeof sectionData === 'object' && !Array.isArray(sectionData)) {
+        subjectForAjv = sectionData as JsonMapType
+      }
+    }
 
     const jsonSchemaParse = jsonSchemaValidate(
       subjectForAjv,