The history of the Resurrection Church is closely linked to the existence of the Resurrection Convent in Bryansk. This ancient convent likely emerged in the 15th-16th centuries when the settlement adjacent to the fortress began to develop actively. Documents from the 17th century indicate the economic poverty of the convent during that period, which necessitated support from other monasteries. Initially, there were two churches in the convent, the Resurrection and the Ascension, as well as 20 monastic cells, but over time only the Resurrection Church remained.

In the early 18th century, active stone construction began in the convent, indicating an improvement in its economic situation. A new stone church was built in honor of the Renewal of the Church of the Resurrection of Christ. In 1706, the abbess of the convent, Kapitolina, appealed to the Patriarchal treasury with a request to consecrate this newly built church. A decree for consecration was issued, and in February 1706, an Antimension was granted. However, soon after this period of prosperity, the convent was abolished, and the recently built church was dismantled due to the events of the Northern War.

In 1713, the restored Resurrection Convent had only one wooden church, but in 1738, the construction of the stone Resurrection Church began, which was completed in 1741. Along with the main altar, a chapel was arranged in the name of the Holy Martyrs Gurias, Samon, and Aviva. In March 1766, the convent was abolished, and the Resurrection Church became a parish church. In 1843, a chapel was arranged in the name of Saint Martyr Andrew the General and a bell tower was built, which was expanded at the lower part in the second half of the 19th century. According to the memories of locals, after the Renovationist schism in 1922, the church was divided between the Orthodox and the Renovationists. In July-August 1937, Orthodox clergy, including the Holy Martyr protodeacon Serafim Vasilenko, were arrested and executed. The church continued to be served by a Renovationist priest and the Renovationist 'Archbishop' of Bryansk, Vladimir Dosychev, but they too were arrested and executed in late 1937 and early 1938. It is likely that after this, the church was closed. Before the start of the fascist occupation, the building was used as a household services combine and a shoemaking workshop; in 1940, the bell tower and dome were demolished, and a second floor was added. Worship services resumed during the war, and by 1985, the church was fully restored to its original appearance.