The first mention of the church dedicated to the Akhtyr Icon of the Mother of God dates back to 1736. Initially, it was a wooden structure located behind the city square and referred to as "behind the orders." In 1782, the church was expanded and rebuilt in the popular Western European architectural style of the time, becoming a single-domed church with a refectory and a three-tiered bell tower.

In 1898, significant reconstruction work was carried out in the church. It became a three-altar church, and its appearance changed completely: elements of "pseudo-Russian style" appeared on the facades, such as decorative zakomaras, kokoshniks, a tent on the bell tower, and twelve bulbous domes.

In the 1920s, the building of the Akhtyr church housed a shelter for a medical institute. From 1937 to 1950, it housed a mattress workshop. In the 1950s, the tiered completion and domes on the main volume were dismantled, as well as the two upper tiers of the bell tower. A floor was added above the first tier with an internal layout corresponding to the new function of the church, a warehouse for medical equipment.

In 1997, the building of the church was returned to the Kursk Diocese of the Russian Orthodox Church.

During the restoration carried out from 2007 to 2014, the domes and bell tower were restored. The foundation was strengthened, the walls of the added second floor were dismantled, and the destroyed arch of the western entrance was restored. The destroyed upper parts of the main volume, kokoshniks, and drums of the domes were also restored. The brick vault of the main volume and the vaulted ceiling of the apse, the lost vault of the apse part, and the second and third tiers of the bell tower were restored. Concrete floors were laid, and the vaults of the destroyed section of the vaulted ceiling in the northern altar were restored. The cornice part of the altar, the narthex, and the altar part were restored, as well as the architectural details of the facades. Restoration of the brickwork of the walls was carried out, frameworks for the bulbous domes were made, and the dome and tent of the bell tower were covered with roofing copper.