The Assumption Cathedral in Kolomna was founded in 1379 by Saint Prince Dmitry Donskoy in honor of the victory of Russian troops over the Golden Horde on the Voga River. In 1380, before the Battle of Kulikovo, the prince prayed in this under-construction church. After the victory, the cathedral was completed and became the main church of the Kolomna Diocese, established in 1353.

The Don Icon of the Mother of God, the church's shrine, accompanied the prince in his feat on Kulikovo Field. This image, created by Theophanes the Greek, was highly revered in Russia. Tsar Ivan the Terrible prayed before it before the Kazan campaign, and after the victory, he took the icon to Moscow, leaving two exact copies for the Kolomna cathedral.

It is believed that Theophanes the Greek participated in the painting of the church in 1392. The lower church had altars in honor of the Assumption of the Mother of God and Saint Dmitry of Thessalonica, while the upper church had altars for Saint Nikita and Saint Leontius of Rostov. The cathedral housed the relics of Saint John the Baptist and the Venerable Stephen of Savva. The church was richly adorned with icons in silver settings and embroidered cloths, one of which was embroidered by Sophia Palaiologina. The cathedral was famous for its library and was the burial place of Kolomna archbishops.

From 1581 to 1586, Saint Job, the first Patriarch of Moscow and all Rus, served here. The cathedral founded by Dmitry Donskoy stood until 1672 when it was dismantled due to dilapidation. In its place, architect Melentius Alekseev built a new five-domed church using the white stone of the old cathedral. At the same time, a tented bell tower was erected adjacent to the Tikhvin Church. In 1804, the cathedral was repainted. In the early 19th century, the rector was Archpriest Mikhail Drozdov, the father of Saint Philaret, who also served and preached here.

In 1880, the cathedral celebrated the 500th anniversary of the Battle of Kulikovo. In the 1820s, the church elder was Dmitry Vdovin, canonized in 2002. In 1929, the church was closed and looted, and the burials of the archpastors were desecrated. In 1989, the cathedral was returned to the faithful, and after restoration, it was consecrated by Patriarch Alexy II on August 29, 1999.