diff --git a/.evergreen/config.in.yml b/.evergreen/config.in.yml
index dd30ee38a3e..df9df455f78 100644
--- a/.evergreen/config.in.yml
+++ b/.evergreen/config.in.yml
@@ -45,15 +45,6 @@ functions:
       params:
         file: src/expansion.yml
 
-  "run search index management tests":
-    - command: subprocess.exec
-      params:
-        binary: bash
-        working_dir: src
-        add_expansions_to_env: true
-        args:
-          - .evergreen/run-search-index-management-tests.sh
-
   "bootstrap mongo-orchestration":
     - command: subprocess.exec
       params:
@@ -1281,6 +1272,19 @@ tasks:
             TEST_LAMBDA_DIRECTORY: ${PROJECT_DIRECTORY}/test/lambda
             AWS_REGION: us-east-1
 
+  - name: test-search-index-helpers
+    commands:
+      - func: install dependencies
+        vars:
+          NODE_LTS_VERSION: 20
+      - command: subprocess.exec
+        params:
+          working_dir: src
+          binary: bash
+          add_expansions_to_env: true
+          args:
+            - .evergreen/run-search-index-management-tests.sh
+
 task_groups:
   - name: serverless_task_group
     setup_group_can_fail_task: true
@@ -1420,6 +1424,8 @@ task_groups:
           working_dir: src
           binary: bash
           add_expansions_to_env: true
+          env:
+            MONGODB_VERSION: "7.0"
           args:
             - ${DRIVERS_TOOLS}/.evergreen/atlas/setup-atlas-cluster.sh
       - command: expansions.update
@@ -1438,6 +1444,34 @@ task_groups:
     tasks:
       - test-aws-lambda-deployed
 
+  - name: test_atlas_task_group_search_indexes
+    setup_group:
+      - func: fetch source
+      - command: subprocess.exec
+        params:
+          working_dir: src
+          binary: bash
+          add_expansions_to_env: true
+          env:
+            MONGODB_VERSION: "7.0"
+          args:
+            - ${DRIVERS_TOOLS}/.evergreen/atlas/setup-atlas-cluster.sh
+      - command: expansions.update
+        params:
+          file: src/atlas-expansion.yml
+    teardown_group:
+      - command: subprocess.exec
+        params:
+          working_dir: src
+          binary: bash
+          add_expansions_to_env: true
+          args:
+            - ${DRIVERS_TOOLS}/.evergreen/atlas/teardown-atlas-cluster.sh
+    setup_group_can_fail_task: true
+    setup_group_timeout_secs: 1800
+    tasks:
+      - test-search-index-helpers
+
 pre:
   - func: "fetch source"
   - func: "windows fix"
diff --git a/.evergreen/config.yml b/.evergreen/config.yml
index 8b1c7752674..55d2fef4b00 100644
--- a/.evergreen/config.yml
+++ b/.evergreen/config.yml
@@ -25,14 +25,6 @@ functions:
     - command: expansions.update
       params:
         file: src/expansion.yml
-  run search index management tests:
-    - command: subprocess.exec
-      params:
-        binary: bash
-        working_dir: src
-        add_expansions_to_env: true
-        args:
-          - .evergreen/run-search-index-management-tests.sh
   bootstrap mongo-orchestration:
     - command: subprocess.exec
       params:
@@ -1204,6 +1196,18 @@ tasks:
           env:
             TEST_LAMBDA_DIRECTORY: ${PROJECT_DIRECTORY}/test/lambda
             AWS_REGION: us-east-1
+  - name: test-search-index-helpers
+    commands:
+      - func: install dependencies
+        vars:
+          NODE_LTS_VERSION: 20
+      - command: subprocess.exec
+        params:
+          working_dir: src
+          binary: bash
+          add_expansions_to_env: true
+          args:
+            - .evergreen/run-search-index-management-tests.sh
   - name: test-latest-server
     tags:
       - latest
@@ -2651,17 +2655,6 @@ tasks:
         variant: '*'
         status: '*'
         patch_optional: true
-  - name: test-search-index-helpers
-    tags: []
-    commands:
-      - func: install dependencies
-        vars:
-          NODE_LTS_NAME: 20
-      - func: bootstrap mongo-orchestration
-        vars:
-          VERSION: latest
-          TOPOLOGY: replica_set
-      - func: run search index management tests
   - name: run-custom-csfle-tests-5.0-pinned-commit
     tags:
       - run-custom-dependency-tests
@@ -3473,6 +3466,8 @@ task_groups:
           working_dir: src
           binary: bash
           add_expansions_to_env: true
+          env:
+            MONGODB_VERSION: '7.0'
           args:
             - ${DRIVERS_TOOLS}/.evergreen/atlas/setup-atlas-cluster.sh
       - command: expansions.update
@@ -3490,6 +3485,33 @@ task_groups:
     setup_group_timeout_secs: 1800
     tasks:
       - test-aws-lambda-deployed
+  - name: test_atlas_task_group_search_indexes
+    setup_group:
+      - func: fetch source
+      - command: subprocess.exec
+        params:
+          working_dir: src
+          binary: bash
+          add_expansions_to_env: true
+          env:
+            MONGODB_VERSION: '7.0'
+          args:
+            - ${DRIVERS_TOOLS}/.evergreen/atlas/setup-atlas-cluster.sh
+      - command: expansions.update
+        params:
+          file: src/atlas-expansion.yml
+    teardown_group:
+      - command: subprocess.exec
+        params:
+          working_dir: src
+          binary: bash
+          add_expansions_to_env: true
+          args:
+            - ${DRIVERS_TOOLS}/.evergreen/atlas/teardown-atlas-cluster.sh
+    setup_group_can_fail_task: true
+    setup_group_timeout_secs: 1800
+    tasks:
+      - test-search-index-helpers
 pre:
   - func: fetch source
   - func: windows fix
@@ -4063,8 +4085,8 @@ buildvariants:
     tasks:
       - test-lambda-example
       - test-lambda-aws-auth-example
-  - name: rhel8-test-seach-index-management-helpers
-    display_name: Search Index Management Helpers Tests
+  - name: rhel8-test-search-indexes
+    display_name: Search Index Tests
     run_on: rhel80-large
     tasks:
-      - test-search-index-helpers
+      - test_atlas_task_group_search_indexes
diff --git a/.evergreen/generate_evergreen_tasks.js b/.evergreen/generate_evergreen_tasks.js
index 2ef05d4fe5c..ecd65967dc8 100644
--- a/.evergreen/generate_evergreen_tasks.js
+++ b/.evergreen/generate_evergreen_tasks.js
@@ -547,6 +547,7 @@ SINGLETON_TASKS.push(
   ]
 );
 
+
 function* makeTypescriptTasks() {
   for (const TS_VERSION of ['next', 'current', '4.1.6']) {
     // 4.1.6 can consume the public API but not compile the driver
@@ -688,26 +689,6 @@ const coverageTask = {
 };
 
 SINGLETON_TASKS.push(coverageTask);
-SINGLETON_TASKS.push({
-  name: 'test-search-index-helpers',
-  tags: [],
-  commands: [
-    {
-      func: 'install dependencies',
-      vars: {
-        NODE_LTS_NAME: LATEST_LTS
-      }
-    },
-    {
-      func: 'bootstrap mongo-orchestration',
-      vars: {
-        VERSION: 'latest',
-        TOPOLOGY: 'replica_set'
-      }
-    },
-    { func: 'run search index management tests' }
-  ]
-})
 SINGLETON_TASKS.push(...oneOffFuncAsTasks);
 
 BUILD_VARIANTS.push({
@@ -776,11 +757,11 @@ BUILD_VARIANTS.push({
 });
 
 BUILD_VARIANTS.push({
-  name: 'rhel8-test-seach-index-management-helpers',
-  display_name: 'Search Index Management Helpers Tests',
+  name: 'rhel8-test-search-indexes',
+  display_name: 'Search Index Tests',
   run_on: DEFAULT_OS,
-  tasks: ['test-search-index-helpers']
-})
+  tasks: ['test_atlas_task_group_search_indexes']
+});
 
 // TODO(NODE-4575): unskip zstd and snappy on node 16
 for (const variant of BUILD_VARIANTS.filter(
diff --git a/.evergreen/run-search-index-management-tests.sh b/.evergreen/run-search-index-management-tests.sh
index 825e5732adf..2dc1f34e5ca 100644
--- a/.evergreen/run-search-index-management-tests.sh
+++ b/.evergreen/run-search-index-management-tests.sh
@@ -1,5 +1,5 @@
 #! /bin/bash
 
-source "${PROJECT_DIRECTORY}/.evergreen/init-nvm.sh"
+source "${PROJECT_DIRECTORY}/.evergreen/init-node-and-npm-env.sh"
 
 npm run check:search-indexes
diff --git a/package.json b/package.json
index 05ce0b5ddd8..db79bde634e 100644
--- a/package.json
+++ b/package.json
@@ -140,7 +140,7 @@
     "check:tsd": "tsd --version && tsd",
     "check:dependencies": "mocha test/action/dependency.test.ts",
     "check:dts": "node ./node_modules/typescript/bin/tsc --noEmit mongodb.d.ts && tsd",
-    "check:search-indexes": "nyc mocha --config test/mocha_mongodb.json test/manual/search-index-management.spec.test.ts",
+    "check:search-indexes": "nyc mocha --config test/mocha_mongodb.json test/manual/search-index-management.prose.test.ts",
     "check:test": "mocha --config test/mocha_mongodb.json test/integration",
     "check:unit": "mocha test/unit",
     "check:ts": "node ./node_modules/typescript/bin/tsc -v && node ./node_modules/typescript/bin/tsc --noEmit",
diff --git a/src/operations/search_indexes/drop.ts b/src/operations/search_indexes/drop.ts
index e9ba3cfa48b..5f29308f86e 100644
--- a/src/operations/search_indexes/drop.ts
+++ b/src/operations/search_indexes/drop.ts
@@ -1,6 +1,7 @@
 import type { Document } from 'bson';
 
 import type { Collection } from '../../collection';
+import { MONGODB_ERROR_CODES, MongoServerError } from '../../error';
 import type { Server } from '../../sdam/server';
 import type { ClientSession } from '../../sessions';
 import { AbstractOperation } from '../operation';
@@ -22,7 +23,14 @@ export class DropSearchIndexOperation extends AbstractOperation<void> {
       command.name = this.name;
     }
 
-    await server.commandAsync(namespace, command, { session });
-    return;
+    try {
+      await server.commandAsync(namespace, command, { session });
+    } catch (error) {
+      const isNamespaceNotFoundError =
+        error instanceof MongoServerError && error.code === MONGODB_ERROR_CODES.NamespaceNotFound;
+      if (!isNamespaceNotFoundError) {
+        throw error;
+      }
+    }
   }
 }
diff --git a/test/manual/search-index-management.spec.test.ts b/test/integration/index-management/search-index-management.spec.test.ts
similarity index 57%
rename from test/manual/search-index-management.spec.test.ts
rename to test/integration/index-management/search-index-management.spec.test.ts
index ce7b7958fe6..f519605f690 100644
--- a/test/manual/search-index-management.spec.test.ts
+++ b/test/integration/index-management/search-index-management.spec.test.ts
@@ -1,7 +1,7 @@
 import { join } from 'path';
 
-import { loadSpecTests } from '../spec';
-import { runUnifiedSuite } from '../tools/unified-spec-runner/runner';
+import { loadSpecTests } from '../../spec';
+import { runUnifiedSuite } from '../../tools/unified-spec-runner/runner';
 
 describe('Search Index Management Tests (Unified)', function () {
   runUnifiedSuite(loadSpecTests(join('index-management')));
diff --git a/test/manual/search-index-management.prose.test.ts b/test/manual/search-index-management.prose.test.ts
new file mode 100644
index 00000000000..4e676ee34e2
--- /dev/null
+++ b/test/manual/search-index-management.prose.test.ts
@@ -0,0 +1,287 @@
+import { expect } from 'chai';
+import { lt } from 'semver';
+import { Readable } from 'stream';
+import { clearTimeout, setTimeout as setTimeoutCb } from 'timers';
+import { setInterval } from 'timers/promises';
+
+import { type Collection, type Document, type MongoClient, ObjectId } from '../mongodb';
+
+class TimeoutController extends AbortController {
+  timeoutId: NodeJS.Timeout;
+  constructor(timeoutMS: number) {
+    super();
+
+    this.timeoutId = setTimeoutCb(() => {
+      this.abort(new Error(`Test timed out after ${timeoutMS} milliseconds.`));
+    }, timeoutMS);
+  }
+
+  clear(abort = false) {
+    if (abort) {
+      this.abort();
+    }
+    clearTimeout(this.timeoutId);
+  }
+}
+
+const metadata: MongoDBMetadataUI = {
+  requires: {
+    mongodb: '>=7.0'
+  }
+};
+
+describe('Index Management Prose Tests', function () {
+  describe('Search Index Management Tests', function () {
+    this.timeout(300000); // set timeout at five minutes
+
+    let client: MongoClient;
+    let timeoutController: TimeoutController;
+    let collection: Collection;
+
+    /**
+     * waits until the search indexes for `collection` satisfy `predicate`.
+     *
+     * This optionally pre-filtering
+     * for indexes with name = `indexName`
+     */
+    function waitForIndexes({
+      predicate,
+      indexNames
+    }: {
+      predicate: (arg0: Array<Document>) => boolean;
+      indexNames: string | string[];
+    }): Promise<Array<Document>> {
+      const names = new Set([indexNames].flat());
+      return Readable.from(
+        setInterval(5000, undefined, { signal: timeoutController.signal, ref: false })
+      )
+        .map(() => collection.listSearchIndexes().toArray())
+        .map((indexes: Document[]) => indexes.filter(index => names.has(index.name)))
+        .find(predicate);
+    }
+
+    before(function () {
+      this.configuration = this.configuration.makeAtlasTestConfiguration();
+    });
+
+    beforeEach(function () {
+      if (lt(process.version, '18.0.0')) {
+        this.currentTest.skipReason = 'Test requires Node18+';
+        this.skip();
+      }
+    });
+
+    beforeEach(async function () {
+      client = this.configuration.newClient();
+      await client.connect();
+
+      // Create a collection with the "create" command using a randomly generated name (referred to as coll0).
+      collection = await client.db('node-test').createCollection(new ObjectId().toHexString());
+
+      timeoutController = new TimeoutController(60 * 1000 * 4);
+    });
+
+    afterEach(async () => {
+      await collection.drop();
+      await client?.close();
+      timeoutController?.clear(false);
+    });
+
+    it(
+      'Case 1: Driver can successfully create and list search indexes',
+      metadata,
+      async function () {
+        // Create a new search index on coll0 with the createSearchIndex helper. Use the following definition:
+        // {
+        //   name: 'test-search-index',
+        //   definition: {
+        //     mappings: { dynamic: false }
+        //   }
+        // }
+        const name = await collection.createSearchIndex({
+          name: 'test-search-index',
+          definition: {
+            mappings: { dynamic: false }
+          }
+        });
+
+        // Assert that the command returns the name of the index: "test-search-index".
+        expect(name).to.equal('test-search-index');
+
+        // Run coll0.listSearchIndexes() repeatedly every 5 seconds until the following condition is satisfied and store the value in a variable index:
+        // 1. An index with the name of test-search-index is present and the index has a field queryable with a value of true.
+        const [index] = await waitForIndexes({
+          predicate: indexes => indexes.every(index => index.queryable),
+          indexNames: 'test-search-index'
+        });
+
+        // Assert that index has a property latestDefinition whose value is { 'mappings': { 'dynamic': false } }
+        expect(index).to.exist;
+        expect(index)
+          .to.have.property('latestDefinition')
+          .to.deep.equal({ mappings: { dynamic: false } });
+      }
+    );
+
+    it(
+      'Case 2: Driver can successfully create multiple indexes in batch',
+      metadata,
+      async function () {
+        // Create two new search indexes on coll0 with the createSearchIndexes helper. Use the following definitions when creating the indexes. These definitions are referred to as indexDefinitions.
+        // {
+        //   name: 'test-search-index-1',
+        //   definition: {
+        //     mappings: { dynamic: false }
+        //   }
+        // }
+        // {
+        //   name: 'test-search-index-2',
+        //   definition: {
+        //     mappings: { dynamic: false }
+        //   }
+        // }
+        const indexDefinitions = [
+          {
+            name: 'test-search-index-1',
+            definition: {
+              mappings: { dynamic: false }
+            }
+          },
+          {
+            name: 'test-search-index-2',
+            definition: {
+              mappings: { dynamic: false }
+            }
+          }
+        ];
+
+        const names = await collection.createSearchIndexes(indexDefinitions);
+
+        // Assert that the command returns an array containing the new indexes' names: ["test-search-index-1", "test-search-index-2"].
+        expect(names).to.deep.equal(['test-search-index-1', 'test-search-index-2']);
+
+        // Run coll0.listSearchIndexes() repeatedly every 5 seconds until the following condition is satisfied.
+        // 1. An index with the name of test-search-index-1 is present and index has a field queryable with the value of true. Store result in index1.
+        // 2. An index with the name of test-search-index-2 is present and index has a field queryable with the value of true. Store result in index2.
+        const indexes = await waitForIndexes({
+          predicate: indexes => indexes.every(index => index.queryable),
+          indexNames: ['test-search-index-1', 'test-search-index-2']
+        });
+
+        const index1 = indexes.find(({ name }) => name === 'test-search-index-1');
+        const index2 = indexes.find(({ name }) => name === 'test-search-index-2');
+
+        // Assert that index1 and index2 have the property latestDefinition whose value is { "mappings" : { "dynamic" : false } }
+        expect(index1)
+          .to.have.property('latestDefinition')
+          .to.deep.equal({ mappings: { dynamic: false } });
+        expect(index2)
+          .to.have.property('latestDefinition')
+          .to.deep.equal({ mappings: { dynamic: false } });
+      }
+    );
+
+    it('Case 3: Driver can successfully drop search indexes', metadata, async function () {
+      // Create a new search index on coll0 with the following definition:
+      // {
+      //   name: 'test-search-index',
+      //   definition: {
+      //     mappings: { dynamic: false }
+      //   }
+      // }
+      const name = await collection.createSearchIndex({
+        name: 'test-search-index',
+        definition: {
+          mappings: { dynamic: false }
+        }
+      });
+
+      // Assert that the command returns the name of the index: "test-search-index".
+      expect(name).to.equal('test-search-index');
+
+      // Run coll0.listSearchIndexes() repeatedly every 5 seconds until the following condition is satisfied:
+      // 1. An index with the name of test-search-index is present and index has a field queryable with the value of true.
+      await waitForIndexes({
+        predicate: indexes => indexes.every(index => index.queryable),
+        indexNames: 'test-search-index'
+      });
+
+      // Run a dropSearchIndex on coll0, using test-search-index for the name.
+      await collection.dropSearchIndex('test-search-index');
+
+      // Run coll0.listSearchIndexes() repeatedly every 5 seconds until listSearchIndexes returns an empty array.
+      // This test fails if it times out waiting for the deletion to succeed.
+      const indexes = await waitForIndexes({
+        predicate: indexes => indexes.length === 0,
+        indexNames: 'test-search-index'
+      });
+
+      expect(indexes).to.deep.equal([]);
+    });
+
+    it('Case 4: Driver can update a search index', metadata, async function () {
+      // Create a new search index on coll0 with the following definition:
+      // {
+      //   name: 'test-search-index',
+      //   definition: {
+      //     mappings: { dynamic: false }
+      //   }
+      // }
+      const name = await collection.createSearchIndex({
+        name: 'test-search-index',
+        definition: {
+          mappings: { dynamic: false }
+        }
+      });
+
+      // Assert that the command returns the name of the index: "test-search-index".
+      expect(name).to.equal('test-search-index');
+
+      // Run coll0.listSearchIndexes() repeatedly every 5 seconds until the following condition is satisfied:
+      // 1. An index with the name of test-search-index is present and index has a field queryable with the value of true.
+      await waitForIndexes({
+        predicate: indexes => indexes.every(index => index.queryable),
+        indexNames: 'test-search-index'
+      });
+
+      // Run a updateSearchIndex on coll0, using the following definition.
+      // {
+      //   name: 'test-search-index',
+      //   definition: {
+      //     mappings: { dynamic: true }
+      //   }
+      // }
+      await collection.updateSearchIndex('test-search-index', { mappings: { dynamic: true } });
+
+      // Assert that the command does not error and the server responds with a success.
+      // The above command throws on failure.
+
+      // Run coll0.listSearchIndexes() repeatedly every 5 seconds until the following condition is satisfied:
+      // 1. An index with the name of test-search-index is present. This index is referred to as index.
+      // 2. The index has a field queryable with a value of true and has a field status with the value of READY.
+      const [index2] = await waitForIndexes({
+        predicate: indexes => indexes.every(index => index.queryable && index.status === 'READY'),
+        indexNames: 'test-search-index'
+      });
+
+      // Assert that an index is present with the name test-search-index and the definition has a
+      // property latestDefinition whose value is { 'mappings': { 'dynamic': true } }.
+      expect(index2).to.have.property('name', 'test-search-index');
+      expect(index2)
+        .to.have.property('latestDefinition')
+        .to.deep.equal({ mappings: { dynamic: true } });
+    });
+
+    it(
+      'Case 5: `dropSearchIndex` suppresses namespace not found errors',
+      metadata,
+      async function () {
+        // Create a driver-side collection object for a randomly generated collection name. Do not create this collection on the server.
+        const collection = await client.db('node-test').collection(new ObjectId().toHexString());
+
+        // Run a dropSearchIndex command and assert that no error is thrown.
+        await collection.dropSearchIndex('test-search-index');
+      }
+    );
+  });
+});
diff --git a/test/spec/index-management/createSearchIndex.json b/test/spec/index-management/createSearchIndex.json
index da664631e7b..04cffbe9c9f 100644
--- a/test/spec/index-management/createSearchIndex.json
+++ b/test/spec/index-management/createSearchIndex.json
@@ -54,7 +54,8 @@
             }
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
@@ -100,7 +101,8 @@
             }
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
diff --git a/test/spec/index-management/createSearchIndex.yml b/test/spec/index-management/createSearchIndex.yml
index 0eb5c1ab1d3..3f923edaed6 100644
--- a/test/spec/index-management/createSearchIndex.yml
+++ b/test/spec/index-management/createSearchIndex.yml
@@ -31,6 +31,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
@@ -50,6 +51,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
diff --git a/test/spec/index-management/createSearchIndexes.json b/test/spec/index-management/createSearchIndexes.json
index b78b3ea6c87..95dbedde773 100644
--- a/test/spec/index-management/createSearchIndexes.json
+++ b/test/spec/index-management/createSearchIndexes.json
@@ -48,7 +48,8 @@
             "models": []
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
@@ -87,7 +88,8 @@
             ]
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
@@ -135,7 +137,8 @@
             ]
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
diff --git a/test/spec/index-management/createSearchIndexes.yml b/test/spec/index-management/createSearchIndexes.yml
index dc01c1b1668..877fc0fa017 100644
--- a/test/spec/index-management/createSearchIndexes.yml
+++ b/test/spec/index-management/createSearchIndexes.yml
@@ -31,6 +31,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
@@ -51,6 +52,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
@@ -70,6 +72,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
diff --git a/test/spec/index-management/dropSearchIndex.json b/test/spec/index-management/dropSearchIndex.json
index b73447f602c..0f21a5b68db 100644
--- a/test/spec/index-management/dropSearchIndex.json
+++ b/test/spec/index-management/dropSearchIndex.json
@@ -48,7 +48,8 @@
             "name": "test index"
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
diff --git a/test/spec/index-management/dropSearchIndex.yml b/test/spec/index-management/dropSearchIndex.yml
index 5ffef7d17e4..bfd6159281c 100644
--- a/test/spec/index-management/dropSearchIndex.yml
+++ b/test/spec/index-management/dropSearchIndex.yml
@@ -31,6 +31,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
@@ -39,4 +40,3 @@ tests:
                 dropSearchIndex: *collection0
                 name: *indexName
                 $db: *database0
-
diff --git a/test/spec/index-management/listSearchIndexes.json b/test/spec/index-management/listSearchIndexes.json
index 41e2655fb3a..24c51ad88c7 100644
--- a/test/spec/index-management/listSearchIndexes.json
+++ b/test/spec/index-management/listSearchIndexes.json
@@ -45,7 +45,8 @@
           "name": "listSearchIndexes",
           "object": "collection0",
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
@@ -79,7 +80,8 @@
             "name": "test index"
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
@@ -119,7 +121,8 @@
             }
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
diff --git a/test/spec/index-management/listSearchIndexes.yml b/test/spec/index-management/listSearchIndexes.yml
index 7d3c3187b91..c912eae83c0 100644
--- a/test/spec/index-management/listSearchIndexes.yml
+++ b/test/spec/index-management/listSearchIndexes.yml
@@ -29,6 +29,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
@@ -48,6 +49,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
@@ -70,6 +72,7 @@ tests:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
diff --git a/test/spec/index-management/updateSearchIndex.json b/test/spec/index-management/updateSearchIndex.json
index 00cd7e75417..88a46a3069c 100644
--- a/test/spec/index-management/updateSearchIndex.json
+++ b/test/spec/index-management/updateSearchIndex.json
@@ -49,7 +49,8 @@
             "definition": {}
           },
           "expectError": {
-            "isError": true
+            "isError": true,
+            "errorContains": "Search index commands are only supported with Atlas"
           }
         }
       ],
diff --git a/test/spec/index-management/updateSearchIndex.yml b/test/spec/index-management/updateSearchIndex.yml
index 215dbc42f92..03d248b3dc2 100644
--- a/test/spec/index-management/updateSearchIndex.yml
+++ b/test/spec/index-management/updateSearchIndex.yml
@@ -28,10 +28,11 @@ tests:
         arguments:
           name: &indexName 'test index'
           definition: &definition {}
-        expectError:          
+        expectError:
           # Search indexes are only available on 7.0+ atlas clusters.  DRIVERS-2630 will add e2e testing 
           # against an Atlas cluster and the expectError will be removed.
           isError: true
+          errorContains: Search index commands are only supported with Atlas
     expectEvents:
       - client: *client0
         events:
diff --git a/test/tools/runner/config.ts b/test/tools/runner/config.ts
index 375b909a744..a07f6373ccc 100644
--- a/test/tools/runner/config.ts
+++ b/test/tools/runner/config.ts
@@ -74,7 +74,7 @@ export class TestConfiguration {
   };
   serverApi: ServerApi;
 
-  constructor(uri: string, context: Record<string, any>) {
+  constructor(private uri: string, private context: Record<string, any>) {
     const url = new ConnectionString(uri);
     const { hosts } = url;
     const hostAddresses = hosts.map(HostAddress.fromString);
@@ -354,4 +354,25 @@ export class TestConfiguration {
   kmsProviders(localKey): Record<string, any> {
     return { local: { key: localKey } };
   }
+
+  makeAtlasTestConfiguration(): AtlasTestConfiguration {
+    return new AtlasTestConfiguration(this.uri, this.context);
+  }
+}
+
+/**
+ * A specialized configuration used to connect to Atlas for testing.
+ *
+ * This class requires that the Atlas srv URI is set as the `MONGODB_URI` in the environment.
+ */
+export class AtlasTestConfiguration extends TestConfiguration {
+  override newClient(): MongoClient {
+    // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
+    return new MongoClient(process.env.MONGODB_URI!);
+  }
+
+  override url(): string {
+    // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
+    return process.env.MONGODB_URI!;
+  }
 }