The first wooden church in honor of the Resurrection of Christ was built in 1640, coinciding with the founding of the fortress town of Khotmyzhsk. The church housed a gilded silver cross, which Tsar Alexei Mikhailovich gifted in 1649 in honor of the victory in the battle near Khotmyzhsk. Over time, this valuable item was lost. Over two centuries, the church deteriorated significantly and needed major repairs. By that time, the fortress had lost its significance, and the village had become a district town. It was decided to build a new stone church on this site.

In 1835, the construction of a three-altar stone church dedicated to the Resurrection of Christ began in the district town of Khotmyzhsk in the Kursk province, designed by architect Avraam Ivanovich Melnikov in the style of late classicism. The church was consecrated in 1839. Before the revolution, the church was renowned for its magnificent decoration: a four-tiered wooden carved gilded iconostasis made by Italian craftsmen, as well as a chandelier and icon cases made by the same craftsmen.

In the 1930s, the church was looted and closed, later being used as a storage facility for pesticides. In the 1960s, during the Khrushchev persecutions, the bell tower with the colonnade was completely destroyed.

By the mid-1990s, an Orthodox community was established in the village, and in 1995, a decision was made to restore the church. On September 28, 1996, His Holiness Patriarch Alexy II of Moscow and all Rus visited the church, consecrating the Bell of Unity of the Slavic Peoples, installed on the bell tower, and gifting the Kazan Icon of the Mother of God to the church. Since 1997, every two years in September, the International Festival of Slavic Culture and Arts "Khotmyzhsk Autumn" has been held in the Resurrection Church, with delegations from the border regions of Russia, Ukraine, and Belarus participating.