diff --git a/services/github/github-api-provider.integration.js b/services/github/github-api-provider.integration.js
index 4e5832c90ef06..ce02069d2af72 100644
--- a/services/github/github-api-provider.integration.js
+++ b/services/github/github-api-provider.integration.js
@@ -17,11 +17,32 @@ describe('Github API provider', function () {
 
   let githubApiProvider
 
-  context('without token pool', function () {
+  context('with no auth', function () {
     before(function () {
       githubApiProvider = new GithubApiProvider({
         baseUrl,
-        withPooling: false,
+        authType: GithubApiProvider.AUTH_TYPES.NO_AUTH,
+      })
+    })
+
+    it('should be able to run 10 requests', async function () {
+      this.timeout('20s')
+      for (let i = 0; i < 10; ++i) {
+        const { res } = await githubApiProvider.fetch(
+          fetch,
+          '/repos/rust-lang/rust',
+          {},
+        )
+        expect(res.statusCode).to.equal(200)
+      }
+    })
+  })
+
+  context('with global token', function () {
+    before(function () {
+      githubApiProvider = new GithubApiProvider({
+        baseUrl,
+        authType: GithubApiProvider.AUTH_TYPES.GLOBAL_TOKEN,
         globalToken: token,
         reserveFraction,
       })
@@ -30,7 +51,12 @@ describe('Github API provider', function () {
     it('should be able to run 10 requests', async function () {
       this.timeout('20s')
       for (let i = 0; i < 10; ++i) {
-        await githubApiProvider.fetch(fetch, '/repos/rust-lang/rust', {})
+        const { res } = await githubApiProvider.fetch(
+          fetch,
+          '/repos/rust-lang/rust',
+          {},
+        )
+        expect(res.statusCode).to.equal(200)
       }
     })
   })
@@ -40,7 +66,7 @@ describe('Github API provider', function () {
     before(function () {
       githubApiProvider = new GithubApiProvider({
         baseUrl,
-        withPooling: true,
+        authType: GithubApiProvider.AUTH_TYPES.TOKEN_POOL,
         reserveFraction,
       })
       githubApiProvider.addToken(token)
diff --git a/services/github/github-api-provider.js b/services/github/github-api-provider.js
index a37513761b1a9..520daa6533e56 100644
--- a/services/github/github-api-provider.js
+++ b/services/github/github-api-provider.js
@@ -33,11 +33,17 @@ const bodySchema = Joi.object({
 
 // Provides an interface to the Github API. Manages the base URL.
 class GithubApiProvider {
+  static AUTH_TYPES = {
+    NO_AUTH: 'No Auth',
+    GLOBAL_TOKEN: 'Global Token',
+    TOKEN_POOL: 'Token Pool',
+  }
+
   // reserveFraction: The amount of much of a token's quota we avoid using, to
   //   reserve it for the user.
   constructor({
     baseUrl,
-    withPooling = true,
+    authType,
     onTokenInvalidated = tokenString => {},
     globalToken,
     reserveFraction = 0.25,
@@ -45,13 +51,13 @@ class GithubApiProvider {
   }) {
     Object.assign(this, {
       baseUrl,
-      withPooling,
+      authType,
       onTokenInvalidated,
       globalToken,
       reserveFraction,
     })
 
-    if (this.withPooling) {
+    if (this.authType === this.constructor.AUTH_TYPES.TOKEN_POOL) {
       this.standardTokens = new TokenPool({ batchSize: 25 })
       this.searchTokens = new TokenPool({ batchSize: 5 })
       this.graphqlTokens = new TokenPool({ batchSize: 25 })
@@ -60,7 +66,7 @@ class GithubApiProvider {
   }
 
   addToken(tokenString) {
-    if (this.withPooling) {
+    if (this.authType === this.constructor.AUTH_TYPES.TOKEN_POOL) {
       this.standardTokens.add(tokenString)
       this.searchTokens.add(tokenString)
       this.graphqlTokens.add(tokenString)
@@ -157,7 +163,7 @@ class GithubApiProvider {
 
     let token
     let tokenString
-    if (this.withPooling) {
+    if (this.authType === this.constructor.AUTH_TYPES.TOKEN_POOL) {
       try {
         token = this.tokenForUrl(url)
       } catch (e) {
@@ -167,7 +173,7 @@ class GithubApiProvider {
         })
       }
       tokenString = token.id
-    } else {
+    } else if (this.authType === this.constructor.AUTH_TYPES.GLOBAL_TOKEN) {
       tokenString = this.globalToken
     }
 
@@ -176,14 +182,20 @@ class GithubApiProvider {
       ...{
         headers: {
           'User-Agent': userAgent,
-          Authorization: `token ${tokenString}`,
           'X-GitHub-Api-Version': this.restApiVersion,
           ...options.headers,
         },
       },
     }
+    if (
+      this.authType === this.constructor.AUTH_TYPES.TOKEN_POOL ||
+      this.authType === this.constructor.AUTH_TYPES.GLOBAL_TOKEN
+    ) {
+      mergedOptions.headers.Authorization = `token ${tokenString}`
+    }
+
     const response = await requestFetcher(`${baseUrl}${url}`, mergedOptions)
-    if (this.withPooling) {
+    if (this.authType === this.constructor.AUTH_TYPES.TOKEN_POOL) {
       if (response.res.statusCode === 401) {
         this.invalidateToken(token)
       } else if (response.res.statusCode < 500) {
diff --git a/services/github/github-auth-service.js b/services/github/github-auth-service.js
index b26bec191cb67..67f249f02c9e5 100644
--- a/services/github/github-auth-service.js
+++ b/services/github/github-auth-service.js
@@ -63,7 +63,14 @@ class GithubAuthV4Service extends BaseGraphqlService {
       `,
     )
 
-    return super._requestGraphql({ ...attrs, ...{ url, query } })
+    return super._requestGraphql({
+      ...attrs,
+      ...{
+        url,
+        query,
+        httpErrorMessages: { 401: 'auth required for graphql api' },
+      },
+    })
   }
 }
 
diff --git a/services/github/github-constellation.js b/services/github/github-constellation.js
index 75754b6c2bcd0..cafdb52d0d18c 100644
--- a/services/github/github-constellation.js
+++ b/services/github/github-constellation.js
@@ -23,19 +23,28 @@ class GithubConstellation {
     this._debugEnabled = config.service.debug.enabled
     this._debugIntervalSeconds = config.service.debug.intervalSeconds
 
+    let authType = GithubApiProvider.AUTH_TYPES.NO_AUTH
+
     const { postgres_url: pgUrl, gh_token: globalToken } = config.private
     if (pgUrl) {
-      log.log('Token persistence configured with dbUrl')
+      log.log('Github Token persistence configured with pgUrl')
       this.persistence = new SqlTokenPersistence({
         url: pgUrl,
         table: 'github_user_tokens',
       })
+      authType = GithubApiProvider.AUTH_TYPES.TOKEN_POOL
+    }
+
+    if (globalToken) {
+      authType = GithubApiProvider.AUTH_TYPES.GLOBAL_TOKEN
     }
 
+    log.log(`Github using auth type: ${authType}`)
+
     this.apiProvider = new GithubApiProvider({
       baseUrl: config.service.baseUri,
       globalToken,
-      withPooling: !globalToken,
+      authType,
       onTokenInvalidated: tokenString => this.onTokenInvalidated(tokenString),
       restApiVersion: config.service.restApiVersion,
     })
@@ -52,7 +61,7 @@ class GithubConstellation {
   }
 
   async initialize(server) {
-    if (!this.apiProvider.withPooling) {
+    if (this.apiProvider.authType !== GithubApiProvider.AUTH_TYPES.TOKEN_POOL) {
       return
     }
 
diff --git a/services/github/github-search.service.js b/services/github/github-search.service.js
index 69ace99dd0309..cd50e6abdb468 100644
--- a/services/github/github-search.service.js
+++ b/services/github/github-search.service.js
@@ -2,7 +2,7 @@ import Joi from 'joi'
 import { metric } from '../text-formatters.js'
 import { nonNegativeInteger } from '../validators.js'
 import { GithubAuthV3Service } from './github-auth-service.js'
-import { httpErrorsFor, documentation } from './github-helpers.js'
+import { documentation } from './github-helpers.js'
 
 const schema = Joi.object({ total_count: nonNegativeInteger }).required()
 
@@ -49,7 +49,11 @@ export default class GithubSearch extends GithubAuthV3Service {
         },
       },
       schema,
-      httpErrors: httpErrorsFor('repo not found'),
+      httpErrors: {
+        401: 'auth required for search api',
+        404: 'repo not found',
+        422: 'repo not found',
+      },
     })
     return this.constructor.render({ query, totalCount })
   }