The first wooden cathedral was built in the Khoperskaya fortress simultaneously with its founding in 1716. The history of the current cathedral in honor of the Resurrection of Christ begins on October 10, 1865, when it was consecrated by Bishop Seraphim of Voronezh and Zadonsk. The new cathedral was erected near the old Cross Exaltation Cathedral, built in 1774, which could no longer accommodate all the parishioners. The main responsibility for the construction fell on the elder and the new Khoper merchant Vasily Mikhailovich Stepanov, who managed to unite the efforts of many wealthy individuals.

Initially, the church had several chapels: the Resurrection of Christ, the Nativity of the Most Holy Theotokos, and the Holy Apostles Peter and Paul. One of the chapels was consecrated in honor of the icon of the Most Holy Theotokos "Quick to Hear," the icon for which was gifted by one of the Athos monasteries in 1863, shortly before the consecration of the church. Contemporaries noted that "the zeal for this icon was so great" that pilgrims came from afar to it. During the Soviet era, after the church was closed, the icon was kept by the faithful and became quite worn, but it was restored by the schemamonk Agnia (Starodubtseva), who lived in silence from 1929 to 1952. Today, this icon is especially venerated by the parishioners of the cathedral.

The church also houses an ancient depiction of St. Nicholas the Wonderworker, brought in 1841 from the Russian Panteleimon Monastery on Mount Athos.

Since the consecration of the Resurrection Church, Zachariah Lavrentyovich Povorinsky served there for 50 years, first as a psalmist and from 1865 as a deacon-psalmist. From the early 1920s until 1927, there existed the Novokhopersk vicarage of the Voronezh diocese, headed by Bishop Paul (Krylov), whose see was located in the Resurrection Cathedral.

After the 1917 revolution, the number of serving priests and church attendants decreased from three to one. In 1922, church valuables were confiscated from the church. However, the problems did not end there: the Renovationist schism further weakened the parish. From 1936 to 1941, the cathedral, having lost its grandeur, was closed and used as a grain warehouse. Only in the 1956-1960s, thanks to the efforts of the rector and the elder of the parish, a major renovation was carried out, the walls were partially painted, icons were restored, and columns were decorated.

Today, the Resurrection Cathedral is the main adornment of the city of Novokhopersk. The five-domed cross-shaped church in the Russian style was designed by architect K. Ton. The compact building is designed for a panoramic view: the arms of the cross are topped with large tent-like kokoshniks, and the elongated western part forms a narthex. The crossing is adorned with a large cylindrical light drum topped with an onion dome. The smaller corner onion domes are octagonal and blind. Twenty meters west of the church stands a slender three-tiered bell tower with a through arch leading to the church grounds. It is crowned with an onion dome, and small domes are placed above the side volumes of the bell tower. On the north side, a one-story priest's house, also built in the 19th century, is included in the complex's composition. The large-scale decor in the Russian style, including kokoshniks, weights, panels, round windows, and niches with icons, emphasizes the majestic architecture of the Resurrection Church. To the south of the bell tower, the construction of a two-story building with a Sunday school is nearing completion, its architecture harmonizing with the historical buildings of the complex.