In the 17th century, there was a male Nicholas Monastery in Kasimov. The wooden church of Nicholas the Wonderworker in this monastery is already mentioned in the land books of Peter Voeykov from 1627. In 1705, with the blessing of Metropolitan Stefan Yavorsky, a townsman named Yakov Petrov Yatskov built a stone church with an altar dedicated to John the Warrior. A stone bell tower with four bells weighing from 1 to 5 poods was added to the church. In 1778, the monastery was abolished, and an invalid team of 60 households was assigned to the remaining church.

The residents did not want to forget about the monastery, and with the permission of the diocesan authorities, on May 9, they began to hold a procession from the cathedral church to the Nicholas church. Until 1832, there was an altar in the church in honor of Saint Dimitri of Rostov, which was abolished, but in 1851 it was restored and also dedicated to Saint Mitrophan of Voronezh. In 1867, the refectory was expanded, and a new bell tower was built. The Nicholas church in Kasimov has always been considered the oldest. A historical document noted that the church was 'dark, as it has little light, but is distinguished by its beauty.'

The icon of Nicholas the Wonderworker, where the Saint is depicted in archpriest vestments with a sword in his right hand and a church in his left, was especially venerated by the parishioners.

On the eastern side of the church, there was a stone chapel where Peter Semyonov was buried, who spent 8 years as a novice in the Sarov Desert with St. Seraphim of Sarov. He died at the age of 124 and was buried with honors.

In 1922, valuables were confiscated from the church to aid the starving Volga region, and an act was drawn up regarding this. The church was closed in 1941, but two years later it was reopened and has not been closed since. From 1944 to 2002, the church effectively served as a cathedral.

Currently, the right altar is dedicated to Saints Dimitri of Rostov and Mitrophan of Voronezh, while the left is dedicated to the martyr John the Warrior.