The Church of St. Nicholas, mentioned in the inventory of 1626 as "the church of Nicholas the Wonderworker in the city," was originally located in the city square within the fortress. In 1775-1779, it was moved to its current location in Kozya Slobodka, built of stone with public donations.

Initially, the church was small and had one altar. In 1844, a refectory was added with two chapels in honor of the Tikhvin Icon of the Mother of God and the Moscow saints Peter, Alexius, Jonah, Philip, and Hermogenes, as well as a bell tower that became the dominant feature of the ensemble. It, made in the traditions of ancient Russian architecture, harmoniously blends with the ancient church.

The church is executed in the style of provincial classicism. To the two-light square with a cross vault and one dome, a lowered volume of the altar with a wide apse, semi-circular vault, and side relieving arches is attached. The altar is separated from the church by a solid stone wall with three arched passages. The refectory and bell tower are built in an eclectic style. The church, in cubic form (without the refectory), has a four-pitched roof and a semi-circular tent. The bell tower is three-tiered, resembling a massive column with a large onion-shaped dome.

The improvement of the church is largely associated with the Kaluga merchant Fyodor Andronovich Izvekov, the church elder, who donated items and money totaling 600 rubles to the church. In 1899-1900, with his funds, the refectory was repaired, the walls of the church were repainted (the paintings were preserved until 1983), and the iconostases were gilded. In 1905-1906, the floors were covered with Mettlach tiles.

In 1848, a church parish school opened at the church.

From July 17, 1935, until his martyr's death in 1937, the rector was the holy martyr archimandrite Joanniky (Dmitriev).

The St. Nicholas Church has rich decorations. All iconostases have been preserved. The main, tall, five-tiered one was created in the late 18th century. Most of the icons are made in the ancient Russian tradition with elements of Western influence. The two-tiered iconostases of the chapels contain both modern and earlier icons. In the local row of the main iconostasis is an ancient life icon of St. Nicholas, transferred from the previous wooden church and particularly venerated by the parishioners. The church also houses icons from closed Kaluga churches. In front of the right choir near the solea is an icon of the Annunciation of the Most Holy Theotokos from the first half of the 18th century from the destroyed Annunciation Church.

The venerated icons of the church include: the icon of St. Nicholas in the iconostasis of the Tikhvin chapel, the Kaluga Icon of the Mother of God, the Kazan Icon of the Mother of God, the icon of the Mother of God "Heal My Sorrows," the icon of the martyrs and confessors Guriy, Samon, and Aviva, the Korsun Icon of the Mother of God, and the icon of the saints Zosima and Savvatiy of Solovetsky.

Archbishop Georgy of Lyudinov (Gryaznov) (1934-2011) is buried in the church's crypt.