diff --git a/lib/connection.js b/lib/connection.js
index 61d325a9dd2..5b3d12af85f 100644
--- a/lib/connection.js
+++ b/lib/connection.js
@@ -550,8 +550,8 @@ Connection.prototype.dropDatabase = _wrapConnHelper(function dropDatabase(cb) {
   // init-ed. It is sufficiently common to call `dropDatabase()` after
   // `mongoose.connect()` but before creating models that we want to
   // support this. See gh-6796
-  for (const name of Object.keys(this.models)) {
-    delete this.models[name].$init;
+  for (const model of Object.values(this.models)) {
+    delete model.$init;
   }
   this.db.dropDatabase(cb);
 });
@@ -838,6 +838,11 @@ Connection.prototype.openUri = function(uri, options, callback) {
     );
   }
 
+  for (const model of Object.values(this.models)) {
+    // Errors handled internally, so safe to ignore error
+    model.init(function $modelInitNoop() {});
+  }
+
   return this.$initialConnection;
 };
 
@@ -951,6 +956,13 @@ Connection.prototype.close = function(force, callback) {
     this.$wasForceClosed = !!force;
   }
 
+  for (const model of Object.values(this.models)) {
+    // If manually disconnecting, make sure to clear each model's `$init`
+    // promise, so Mongoose knows to re-run `init()` in case the
+    // connection is re-opened. See gh-12047.
+    delete model.$init;
+  }
+
   return promiseOrCallback(callback, cb => {
     this._close(force, false, cb);
   });
@@ -1443,6 +1455,11 @@ Connection.prototype.setClient = function setClient(client) {
   this._connectionString = client.s.url;
   _setClient(this, client, {}, client.s.options.dbName);
 
+  for (const model of Object.values(this.models)) {
+    // Errors handled internally, so safe to ignore error
+    model.init(function $modelInitNoop() {});
+  }
+
   return this;
 };
 
diff --git a/test/connection.test.js b/test/connection.test.js
index 332fb8e05af..befcbcef1d6 100644
--- a/test/connection.test.js
+++ b/test/connection.test.js
@@ -1135,6 +1135,72 @@ describe('connections:', function() {
     assert.deepStrictEqual(conn3.id, m.connection.id + 2);
   });
 
+  describe('Automatic init', function() {
+    it('re-runs init() if connecting after disconnecting (gh-12047)', async function() {
+      const conn = await mongoose.createConnection(start.uri).asPromise();
+
+      const Test = conn.model('Test', new Schema({ name: { type: String, index: true } }));
+      await Test.init();
+
+      let indexes = await Test.collection.listIndexes().toArray();
+      assert.equal(indexes.length, 2);
+      assert.equal(indexes[1].name, 'name_1');
+
+      await conn.db.dropCollection(Test.collection.collectionName);
+
+      const err = await Test.collection.listIndexes().toArray().then(() => null, err => err);
+      assert.ok(err);
+      assert.equal(err.codeName, 'NamespaceNotFound');
+
+      await conn.close();
+
+      await conn.openUri(start.uri);
+      assert.ok(Test.$init);
+      await Test.init();
+
+      indexes = await Test.collection.listIndexes().toArray();
+      assert.equal(indexes.length, 2);
+      assert.equal(indexes[1].name, 'name_1');
+    });
+
+    it('re-runs init() if running setClient() after disconnecting (gh-12047)', async function() {
+      const conn = await mongoose.createConnection(start.uri).asPromise();
+
+      const Test = conn.model('Test', new Schema({ name: { type: String, index: true } }));
+      await Test.init();
+
+      let indexes = await Test.collection.listIndexes().toArray();
+      assert.equal(indexes.length, 2);
+      assert.equal(indexes[1].name, 'name_1');
+
+      await conn.db.dropCollection(Test.collection.collectionName);
+
+      const err = await Test.collection.listIndexes().toArray().then(() => null, err => err);
+      assert.ok(err);
+      assert.equal(err.codeName, 'NamespaceNotFound');
+
+      await conn.close();
+
+      const client = await mongodb.MongoClient.connect(start.uri);
+
+      try {
+        conn.setClient(client);
+        assert.ok(Test.$init);
+        await Test.init();
+
+        indexes = await Test.collection.listIndexes().toArray();
+        assert.equal(indexes.length, 2);
+        assert.equal(indexes[1].name, 'name_1');
+
+        await client.close();
+      } catch (err) {
+        await client.close().catch(() => {});
+
+        throw err;
+      }
+    });
+  });
+
   describe('Connection#syncIndexes() (gh-10893) (gh-11039)', () => {
     let connection;
     this.beforeEach(async() => {