diff --git a/src/cmap/connection.ts b/src/cmap/connection.ts
index 1647638045..416b0ee855 100644
--- a/src/cmap/connection.ts
+++ b/src/cmap/connection.ts
@@ -655,8 +655,9 @@ function streamIdentifier(stream: Stream, options: ConnectionOptions): string {
     return options.hostAddress.toString();
   }
 
-  if (typeof stream.address === 'function') {
-    return `${stream.remoteAddress}:${stream.remotePort}`;
+  const { remoteAddress, remotePort } = stream;
+  if (typeof remoteAddress === 'string' && typeof remotePort === 'number') {
+    return HostAddress.fromHostPort(remoteAddress, remotePort).toString();
   }
 
   return uuidV4().toString('hex');
diff --git a/src/sdam/server_description.ts b/src/sdam/server_description.ts
index 541752cb43..ab5da450a1 100644
--- a/src/sdam/server_description.ts
+++ b/src/sdam/server_description.ts
@@ -88,8 +88,8 @@ export class ServerDescription {
 
     this.address =
       typeof address === 'string'
-        ? HostAddress.fromString(address).toString(false) // Use HostAddress to normalize
-        : address.toString(false);
+        ? HostAddress.fromString(address).toString() // Use HostAddress to normalize
+        : address.toString();
     this.type = parseServerType(hello, options);
     this.hosts = hello?.hosts?.map((host: string) => host.toLowerCase()) ?? [];
     this.passives = hello?.passives?.map((host: string) => host.toLowerCase()) ?? [];
diff --git a/src/utils.ts b/src/utils.ts
index 62a2bd6f88..2859132dc4 100644
--- a/src/utils.ts
+++ b/src/utils.ts
@@ -1142,44 +1142,55 @@ export class BufferPool {
 
 /** @public */
 export class HostAddress {
-  host;
-  port;
+  host: string | undefined;
+  port: number | undefined;
   // Driver only works with unix socket path to connect
   // SDAM operates only on tcp addresses
-  socketPath;
-  isIPv6;
+  socketPath: string | undefined;
+  isIPv6 = false;
 
   constructor(hostString: string) {
     const escapedHost = hostString.split(' ').join('%20'); // escape spaces, for socket path hosts
-    const { hostname, port } = new URL(`mongodb://${escapedHost}`);
 
     if (escapedHost.endsWith('.sock')) {
       // heuristically determine if we're working with a domain socket
       this.socketPath = decodeURIComponent(escapedHost);
-    } else if (typeof hostname === 'string') {
-      this.isIPv6 = false;
+      delete this.port;
+      delete this.host;
+      return;
+    }
 
-      let normalized = decodeURIComponent(hostname).toLowerCase();
-      if (normalized.startsWith('[') && normalized.endsWith(']')) {
-        this.isIPv6 = true;
-        normalized = normalized.substring(1, hostname.length - 1);
-      }
+    const urlString = `iLoveJS://${escapedHost}`;
+    let url;
+    try {
+      url = new URL(urlString);
+    } catch (urlError) {
+      const runtimeError = new MongoRuntimeError(`Unable to parse ${escapedHost} with URL`);
+      runtimeError.cause = urlError;
+      throw runtimeError;
+    }
 
-      this.host = normalized.toLowerCase();
+    const hostname = url.hostname;
+    const port = url.port;
 
-      if (typeof port === 'number') {
-        this.port = port;
-      } else if (typeof port === 'string' && port !== '') {
-        this.port = Number.parseInt(port, 10);
-      } else {
-        this.port = 27017;
-      }
+    let normalized = decodeURIComponent(hostname).toLowerCase();
+    if (normalized.startsWith('[') && normalized.endsWith(']')) {
+      this.isIPv6 = true;
+      normalized = normalized.substring(1, hostname.length - 1);
+    }
 
-      if (this.port === 0) {
-        throw new MongoParseError('Invalid port (zero) with hostname');
-      }
+    this.host = normalized.toLowerCase();
+
+    if (typeof port === 'number') {
+      this.port = port;
+    } else if (typeof port === 'string' && port !== '') {
+      this.port = Number.parseInt(port, 10);
     } else {
-      throw new MongoInvalidArgumentError('Either socketPath or host must be defined.');
+      this.port = 27017;
+    }
+
+    if (this.port === 0) {
+      throw new MongoParseError('Invalid port (zero) with hostname');
     }
     Object.freeze(this);
   }
@@ -1189,15 +1200,12 @@ export class HostAddress {
   }
 
   inspect(): string {
-    return `new HostAddress('${this.toString(true)}')`;
+    return `new HostAddress('${this.toString()}')`;
   }
 
-  /**
-   * @param ipv6Brackets - optionally request ipv6 bracket notation required for connection strings
-   */
-  toString(ipv6Brackets = false): string {
+  toString(): string {
     if (typeof this.host === 'string') {
-      if (this.isIPv6 && ipv6Brackets) {
+      if (this.isIPv6) {
         return `[${this.host}]:${this.port}`;
       }
       return `${this.host}:${this.port}`;
diff --git a/test/integration/crud/misc_cursors.test.js b/test/integration/crud/misc_cursors.test.js
index 60abe2c757..e8cea657f5 100644
--- a/test/integration/crud/misc_cursors.test.js
+++ b/test/integration/crud/misc_cursors.test.js
@@ -264,39 +264,21 @@ describe('Cursor', function () {
     }
   });
 
-  it('Should correctly execute cursor count with secondary readPreference', {
-    // Add a tag that our runner can trigger on
-    // in this case we are setting that node needs to be higher than 0.10.X to run
-    metadata: {
-      requires: { topology: 'replicaset' }
-    },
-
-    test: function (done) {
-      const configuration = this.configuration;
-      const client = configuration.newClient(configuration.writeConcernMax(), {
-        maxPoolSize: 1,
-        monitorCommands: true
-      });
-
+  it('should correctly execute cursor count with secondary readPreference', {
+    metadata: { requires: { topology: 'replicaset' } },
+    async test() {
       const bag = [];
       client.on('commandStarted', filterForCommands(['count'], bag));
 
-      client.connect((err, client) => {
-        expect(err).to.not.exist;
-        this.defer(() => client.close());
-
-        const db = client.db(configuration.db);
-        const cursor = db.collection('countTEST').find({ qty: { $gt: 4 } });
-        cursor.count({ readPreference: ReadPreference.SECONDARY }, err => {
-          expect(err).to.not.exist;
-
-          const selectedServerAddress = bag[0].address.replace('127.0.0.1', 'localhost');
-          const selectedServer = client.topology.description.servers.get(selectedServerAddress);
-          expect(selectedServer).property('type').to.equal(ServerType.RSSecondary);
+      const cursor = client
+        .db()
+        .collection('countTEST')
+        .find({ qty: { $gt: 4 } });
+      await cursor.count({ readPreference: ReadPreference.SECONDARY });
 
-          done();
-        });
-      });
+      const selectedServerAddress = bag[0].address.replace('127.0.0.1', 'localhost');
+      const selectedServer = client.topology.description.servers.get(selectedServerAddress);
+      expect(selectedServer).property('type').to.equal(ServerType.RSSecondary);
     }
   });
 
diff --git a/test/integration/node-specific/ipv6.test.ts b/test/integration/node-specific/ipv6.test.ts
new file mode 100644
index 0000000000..639a37cc6a
--- /dev/null
+++ b/test/integration/node-specific/ipv6.test.ts
@@ -0,0 +1,91 @@
+import { expect } from 'chai';
+import * as net from 'net';
+import * as process from 'process';
+import * as sinon from 'sinon';
+
+import { ConnectionCreatedEvent, ReadPreference, TopologyType } from '../../../src';
+import { byStrings, sorted } from '../../tools/utils';
+
+describe('IPv6 Addresses', () => {
+  let client;
+  let ipv6Hosts;
+
+  beforeEach(async function () {
+    if (
+      process.platform !== 'win32' ||
+      this.configuration.topologyType !== TopologyType.ReplicaSetWithPrimary
+    ) {
+      if (this.currentTest) {
+        // Ubuntu 18 does not support localhost AAAA lookups (IPv6)
+        // Windows (VS2019) has the AAAA lookup
+        // We do not run a replica set on macos
+        this.currentTest.skipReason =
+          'We are only running this on windows currently because it has the IPv6 translation for localhost';
+      }
+      return this.skip();
+    }
+
+    ipv6Hosts = this.configuration.options.hostAddresses.map(({ port }) => `[::1]:${port}`);
+    client = this.configuration.newClient(`mongodb://${ipv6Hosts.join(',')}/test`, {
+      [Symbol.for('@@mdb.skipPingOnConnect')]: true,
+      maxPoolSize: 1
+    });
+  });
+
+  afterEach(async function () {
+    sinon.restore();
+    await client?.close();
+  });
+
+  it('should have three localhost IPv6 addresses set', function () {
+    const ipv6LocalhostAddresses = this.configuration.options.hostAddresses.map(({ port }) => ({
+      host: '::1',
+      port,
+      isIPv6: true
+    }));
+    expect(client.options.hosts).to.deep.equal(ipv6LocalhostAddresses);
+  });
+
+  it('should successfully connect using IPv6', async function () {
+    const localhostHosts = this.configuration.options.hostAddresses.map(
+      ({ port }) => `localhost:${port}`
+    );
+    await client.db().command({ ping: 1 });
+    // After running the first command we should receive the hosts back as reported by the mongod in a hello response
+    // mongod will report the bound host address, in this case "localhost"
+    expect(sorted(client.topology.s.description.servers.keys(), byStrings)).to.deep.equal(
+      localhostHosts
+    );
+  });
+
+  it('should createConnection with IPv6 addresses initially then switch to mongodb bound addresses', async () => {
+    const createConnectionSpy = sinon.spy(net, 'createConnection');
+
+    const connectionCreatedEvents: ConnectionCreatedEvent[] = [];
+    client.on('connectionCreated', ev => connectionCreatedEvents.push(ev));
+
+    await client.db().command({ ping: 1 }, { readPreference: ReadPreference.primary });
+
+    const callArgs = createConnectionSpy.getCalls().map(({ args }) => args[0]);
+
+    // This is 7 because we create 3 monitoring connections with ::1, then another 3 with localhost
+    // and then 1 more in the connection pool for the operation, that is why we are checking for the connectionCreated event
+    expect(callArgs).to.be.lengthOf(7);
+    expect(connectionCreatedEvents).to.have.lengthOf(1);
+    expect(connectionCreatedEvents[0]).to.have.property('address').that.includes('localhost');
+
+    for (let index = 0; index < 3; index++) {
+      // The first 3 connections (monitoring) are made using the user provided addresses
+      expect(callArgs[index]).to.have.property('host', '::1');
+    }
+
+    for (let index = 3; index < 6; index++) {
+      // MongoDB sends use back hellos that have the bound address 'localhost'
+      // We make new connection using that address instead
+      expect(callArgs[index]).to.have.property('host', 'localhost');
+    }
+
+    // Operation connection
+    expect(callArgs[6]).to.have.property('host', 'localhost');
+  });
+});
diff --git a/test/tools/cluster_setup.sh b/test/tools/cluster_setup.sh
index 3e665e3867..6507321645 100755
--- a/test/tools/cluster_setup.sh
+++ b/test/tools/cluster_setup.sh
@@ -13,15 +13,15 @@ SHARDED_DIR=${SHARDED_DIR:-$DATA_DIR/sharded_cluster}
 
 if [[ $1 == "replica_set" ]]; then
     mkdir -p $REPLICASET_DIR # user / password
-    mlaunch init --dir $REPLICASET_DIR --auth --username "bob" --password "pwd123" --replicaset --nodes 3 --arbiter --name rs --port 31000 --enableMajorityReadConcern --setParameter enableTestCommands=1
+    mlaunch init --dir $REPLICASET_DIR --ipv6 --auth --username "bob" --password "pwd123" --replicaset --nodes 3 --arbiter --name rs --port 31000 --enableMajorityReadConcern --setParameter enableTestCommands=1
     echo "mongodb://bob:pwd123@localhost:31000,localhost:31001,localhost:31002/?replicaSet=rs"
 elif [[ $1 == "sharded_cluster" ]]; then
     mkdir -p $SHARDED_DIR
-    mlaunch init --dir $SHARDED_DIR --auth --username "bob" --password "pwd123" --replicaset --nodes 3 --name rs --port 51000 --enableMajorityReadConcern --setParameter enableTestCommands=1 --sharded 1 --mongos 2
+    mlaunch init --dir $SHARDED_DIR --ipv6 --auth --username "bob" --password "pwd123" --replicaset --nodes 3 --name rs --port 51000 --enableMajorityReadConcern --setParameter enableTestCommands=1 --sharded 1 --mongos 2
     echo "mongodb://bob:pwd123@localhost:51000,localhost:51001"
 elif [[ $1 == "server" ]]; then
     mkdir -p $SINGLE_DIR
-    mlaunch init --dir $SINGLE_DIR --auth --username "bob" --password "pwd123" --single --setParameter enableTestCommands=1
+    mlaunch init --dir $SINGLE_DIR --ipv6 --auth --username "bob" --password "pwd123" --single --setParameter enableTestCommands=1
     echo "mongodb://bob:pwd123@localhost:27017"
 else
     echo "unsupported topology: $1"
diff --git a/test/tools/cmap_spec_runner.ts b/test/tools/cmap_spec_runner.ts
index 54fc94cfd6..81c081e857 100644
--- a/test/tools/cmap_spec_runner.ts
+++ b/test/tools/cmap_spec_runner.ts
@@ -391,7 +391,10 @@ async function runCmapTest(test: CmapTest, threadContext: ThreadContext) {
   if (expectedError) {
     expect(actualError).to.exist;
     const { type: errorType, message: errorMessage, ...errorPropsToCheck } = expectedError;
-    expect(actualError).to.have.property('name', `Mongo${errorType}`);
+    expect(
+      actualError,
+      `${actualError.name} does not match "Mongo${errorType}", ${actualError.message} ${actualError.stack}`
+    ).to.have.property('name', `Mongo${errorType}`);
     if (errorMessage) {
       if (
         errorMessage === 'Timed out while checking out a connection from connection pool' &&
diff --git a/test/tools/runner/config.ts b/test/tools/runner/config.ts
index f5021963d1..525259ff4b 100644
--- a/test/tools/runner/config.ts
+++ b/test/tools/runner/config.ts
@@ -58,7 +58,7 @@ export class TestConfiguration {
   buildInfo: Record<string, any>;
   options: {
     hosts?: string[];
-    hostAddresses?: HostAddress[];
+    hostAddresses: HostAddress[];
     hostAddress?: HostAddress;
     host?: string;
     port?: number;
diff --git a/test/tools/uri_spec_runner.ts b/test/tools/uri_spec_runner.ts
index f81ef86d3e..555c1fa296 100644
--- a/test/tools/uri_spec_runner.ts
+++ b/test/tools/uri_spec_runner.ts
@@ -1,6 +1,6 @@
 import { expect } from 'chai';
 
-import { MongoAPIError, MongoParseError } from '../../src';
+import { MongoAPIError, MongoParseError, MongoRuntimeError } from '../../src';
 import { MongoClient } from '../../src/mongo_client';
 
 type HostObject = {
@@ -71,6 +71,8 @@ export function executeUriValidationTest(
     } catch (err) {
       if (err instanceof TypeError) {
         expect(err).to.have.property('code').equal('ERR_INVALID_URL');
+      } else if (err instanceof MongoRuntimeError) {
+        expect(err).to.have.nested.property('cause.code').equal('ERR_INVALID_URL');
       } else if (
         // most of our validation is MongoParseError, which does not extend from MongoAPIError
         !(err instanceof MongoParseError) &&
diff --git a/test/unit/connection_string.test.ts b/test/unit/connection_string.test.ts
index 21b603e1b2..a04c64722b 100644
--- a/test/unit/connection_string.test.ts
+++ b/test/unit/connection_string.test.ts
@@ -10,7 +10,8 @@ import {
   MongoAPIError,
   MongoDriverError,
   MongoInvalidArgumentError,
-  MongoParseError
+  MongoParseError,
+  MongoRuntimeError
 } from '../../src/error';
 import { MongoClient, MongoOptions } from '../../src/mongo_client';
 
@@ -573,4 +574,51 @@ describe('Connection String', function () {
       expect(client.s.options).to.have.property(flag, null);
     });
   });
+
+  describe('IPv6 host addresses', () => {
+    it('should not allow multiple unbracketed portless localhost IPv6 addresses', () => {
+      // Note there is no "port-full" version of this test, there's no way to distinguish when a port begins without brackets
+      expect(() => new MongoClient('mongodb://::1,::1,::1/test')).to.throw(
+        /invalid connection string/i
+      );
+    });
+
+    it('should not allow multiple unbracketed portless remote IPv6 addresses', () => {
+      expect(
+        () =>
+          new MongoClient(
+            'mongodb://ABCD:f::abcd:abcd:abcd:abcd,ABCD:f::abcd:abcd:abcd:abcd,ABCD:f::abcd:abcd:abcd:abcd/test'
+          )
+      ).to.throw(MongoRuntimeError);
+    });
+
+    it('should allow multiple bracketed portless localhost IPv6 addresses', () => {
+      const client = new MongoClient('mongodb://[::1],[::1],[::1]/test');
+      expect(client.options.hosts).to.deep.equal([
+        { host: '::1', port: 27017, isIPv6: true },
+        { host: '::1', port: 27017, isIPv6: true },
+        { host: '::1', port: 27017, isIPv6: true }
+      ]);
+    });
+
+    it('should allow multiple bracketed portless localhost IPv6 addresses', () => {
+      const client = new MongoClient(
+        'mongodb://[ABCD:f::abcd:abcd:abcd:abcd],[ABCD:f::abcd:abcd:abcd:abcd],[ABCD:f::abcd:abcd:abcd:abcd]/test'
+      );
+      expect(client.options.hosts).to.deep.equal([
+        { host: 'abcd:f::abcd:abcd:abcd:abcd', port: 27017, isIPv6: true },
+        { host: 'abcd:f::abcd:abcd:abcd:abcd', port: 27017, isIPv6: true },
+        { host: 'abcd:f::abcd:abcd:abcd:abcd', port: 27017, isIPv6: true }
+      ]);
+    });
+
+    it('should allow multiple bracketed port-full IPv6 addresses', () => {
+      const client = new MongoClient('mongodb://[::1]:27018,[::1]:27019,[::1]:27020/test');
+      expect(client.options.hosts).to.deep.equal([
+        { host: '::1', port: 27018, isIPv6: true },
+        { host: '::1', port: 27019, isIPv6: true },
+        { host: '::1', port: 27020, isIPv6: true }
+      ]);
+    });
+  });
 });
diff --git a/test/unit/sdam/server_description.test.ts b/test/unit/sdam/server_description.test.ts
index 83331a1f4c..29de0db89b 100644
--- a/test/unit/sdam/server_description.test.ts
+++ b/test/unit/sdam/server_description.test.ts
@@ -63,9 +63,15 @@ describe('ServerDescription', function () {
     }
   });
 
-  it('should sensibly parse an ipv6 address', function () {
-    const description = new ServerDescription('[ABCD:f::abcd:abcd:abcd:abcd]:27017');
-    expect(description.host).to.equal('abcd:f::abcd:abcd:abcd:abcd');
+  it('should normalize an IPv6 address with brackets and toLowered characters', function () {
+    const description = new ServerDescription('[ABCD:f::abcd:abcd:abcd:abcd]:1234');
+    expect(description.host).to.equal('[abcd:f::abcd:abcd:abcd:abcd]'); // IPv6 Addresses must always be bracketed if there is a port
+    expect(description.port).to.equal(1234);
+  });
+
+  it('should normalize an IPv6 address with brackets and toLowered characters even when the port is omitted', function () {
+    const description = new ServerDescription('[ABCD:f::abcd:abcd:abcd:abcd]');
+    expect(description.host).to.equal('[abcd:f::abcd:abcd:abcd:abcd]');
     expect(description.port).to.equal(27017);
   });