The three-domed cathedral was founded in 1379 by Grand Duke Dmitry Donskoy after the victory of the Russian troops over the Horde in the battle on the River Vozha. The construction lasted a year, and it is believed that the frescoes were created by Theophanes the Greek.

From 1581 to 1586, St. Job, Bishop of Kolomna, served in this church, who became the first patriarch of the Russian church.

The cathedral stood until 1673 when it was dismantled due to dilapidation. In its place, architect Meletius Alekseev built a new church over 10 years, which has survived to this day.

In 1804, the church was repainted. The future saint Philaret arrived for the reopening after the frescoes, accompanying Metropolitan Platon Levshin. In the early 19th century, deacon Mikhail Drozdov, the father of Saint Philaret, served in the Assumption Cathedral. He later became a priest and served in the Trinity Church in Yamskaya Sloboda, Kolomna, now known as the Trinity Church on Repna. Saint Philaret himself often served and preached in this church.

In the 1920s, the church's elder was Dmitry Vdovin, who was canonized by the Russian Orthodox Church in 2002 in the Cathedral of New Martyrs and Confessors of Russia.

In 1929, the church was closed and looted, and the burials of Kolomna archpastors were desecrated.

In 1989, the cathedral was returned to the Russian Orthodox Church.

The rector of the Assumption Cathedral is Priest Ilya Lukyanov. The honorary rector of the cathedral is the spiritual father of the Kolomna Theological Seminary and chairman of the Orthodox Brotherhood named after Dmitry Donskoy in Kolomna, Archpriest Nikolai Kachankin.

The shrine of the church, the Don Icon of the Mother of God, accompanied Grand Duke Dmitry Donskoy in his military feat at Kulikovo Field. The image of the Blessed Virgin Mary, created by the venerable Theophanes the Greek, was highly revered in Russia. Tsar Ivan the Terrible prayed before it before the Kazan campaign. After the victory, he took the miraculous image to Moscow and ordered the creation of two exact copies for the Kolomna Assumption Church.

The cathedral housed relics of St. John the Baptist and St. Stephen Savvaite. The church was richly decorated, had icons in silver settings, and embroidered veils, one of which was embroidered by Grand Duchess Sophia Palaiologina. The cathedral was famous for its extensive library.