The church was built in 1818 with funds from merchant Ivan Nikitich Barykov. The project was developed by the famous Russian architect Abraham Ivanovich Melnikov, who also designed the Spaso-Preobrazhensky Cathedral in Rybinsk, the Imperial Law School in St. Petersburg, and the Potemkin Stairs in Odessa.

The church had three altars: the main one dedicated to the Exaltation of the Holy Cross, and two in the warm refectory, in honor of the Holy Myrrhbearers and Saint Great Martyr Nikita. Due to its rich interior decoration and significant capacity, exceeding that of the old city cathedral, the Exaltation Church served as a cathedral until the 1840s, until the new cathedral in honor of St. Nicholas the Wonderworker was completed.

From January 23 to 25, 1826, the body of Emperor Alexander I was in the church, being transported from Taganrog to St. Petersburg. In memory of this event, members of the royal family gifted a chandelier to the church, and a memorial plaque was installed inside. A. A. Fet described his childhood impressions of the royal funeral in his work "The Early Years of My Life."

In 1897, the church was last majorly renovated. Since 1899, a parish school began operating there, located in a separate wooden building.

The church was closed in 1930. During the war, an aerial bomb destroyed the vaults of the refectory. In 1960, the building was placed under state protection, but city authorities still attempted to demolish it, citing its dilapidation. Fortunately, the church was preserved.

On February 23, 1973, the spire of the bell tower collapsed. Since 1976, restoration work has been periodically carried out in the church, which completely ceased by the early 1990s.

In 1999, the church was handed over to the Orthodox community. Restoration work was initially funded by the parish of the Holy Trinity Church in Mtsensk. In the same year, regular services resumed in the church, with the first Divine Liturgy celebrated on the feast of the Entry of the Most Holy Theotokos into the Temple.

Currently, the church continues to be restored, and services are held there.

Since 2006, a Sunday school has been operating at the church, where about 15 children aged 5 to 13 are taught. Classes are held on Sundays from 11 AM to 2 PM. The children study the basics of Orthodox culture and engage in handicrafts. During school breaks, pilgrimages, excursions, and hikes are organized for them.