The wooden church near the Ivanov Gates of the Kolomna Kremlin existed as early as the 16th century. In the early 18th century, it burned down, and it was decided to build a new stone structure in its place. Work began in 1733, but due to a fire in the city in 1739, it had to be suspended. Construction was completed in 1756. From 1810 to 1828, the church was rebuilt and repainted. The iconostasis was made by goldsmith Yegor Vasilyevich Ikonnikov from Tula, and the wall paintings were done by Kolomna painter Theophan Gavrilovich Dremyazgin and his assistants from Kaluga, Apollon Stepanov and Mitrofan Fyodorov. New icons were painted by F. G. Dremyazgin and Moscow icon painter Pyotr Nikitich Lykov. In 1821, the old bell tower was demolished.

From 1826 to 1846, a new five-tiered bell tower in the Empire style was built, reaching a height of 67 meters, making it one of the tallest buildings in the city. After reconstruction on August 28, 1848, the church was re-consecrated by the Metropolitan of Moscow and Kolomna, Philaret.

In 1865, a square of trading premises was built around the church according to the project of architect I. A. Dagaev. These premises belonged to the church clergy and were rented out to local merchants, which was one of the main sources of income for the church.

In 1930, services in the church ceased. In the 1960s, the trading rows were reconstructed while preserving their original appearance. In 1996, services in the church resumed.

The church and the four-pillar refectory are executed in the style of mature classicism using white stone. The apse with Tuscan order columns stands out particularly. The tall slender bell tower with a spire organizes the central square of the city and plays an important role in the panorama of Old Kolomna. The bell tower is adorned with Ionic columns, vases, and elegant stucco. The church houses a unique stone bas-relief icon from the 16th century, "The Mother of God with the Infant Christ and St. John the Theologian."