According to legend, the first church in Arzamas, dedicated to Archangel Michael, was built on the site of the modern Resurrection Cathedral. This occurred in 1552 by order of Tsar Ivan IV the Terrible. A century later, a new wooden church was constructed in honor of the Resurrection of Christ to replace the dilapidated building. In the 18th century, it was moved to the village of Kostyliha, where it remains today. In its place, a stone five-domed church with an altar in honor of the Great Martyr John the Warrior was erected in 1742.

After the victory over Napoleon, the residents of Arzamas decided to build a new cathedral as a sign of gratitude for Russia's victory and liberation from invasion. A donation box was set up in Cathedral Square, and every citizen sought to contribute. The cathedral, built with public funds, became a symbol of Russia's military glory. Before the revolution, it housed the banner of the Arzamas militia, handed over in 1815 by its commander Fyodor Stremoukhov.

Construction of the cathedral began in 1814 based on the design of architect M.P. Korinfsky and lasted for 28 years. The finishing works and painting continued for 21 years. The cathedral was painted by students of the Arzamas School of Painting, Osip Serebryakov and his son Alexander. The iconostases were made by the Lomakin brothers.

The main altar of the cathedral was consecrated in 1840, while the other altars were consecrated in 1832, 1833, 1834, and 1842.

In 1932, the cathedral was closed and turned into a museum of atheism. However, this helped preserve its original appearance and interior decoration, as well as many relics of Arzamas collected from destroyed churches.

In 1944, during the Great Patriotic War, at the request of the faithful and the intercession of Patriarch Sergius (Stragorodsky), the cathedral was returned to the Nizhny Novgorod diocese, and services resumed.

The parish of the Cathedral of the Resurrection of Christ is located in Arzamas, Nizhny Novgorod region, and is part of the deanery of the city of Arzamas in the Nizhny Novgorod diocese. Currently, the parish includes four churches: the cathedral, the church in honor of the icon of the Mother of God "Life-Giving Spring," the church of the Kazan icon of the Mother of God, and an attached church in honor of the Protection of the Most Holy Theotokos in the Arzamas educational colony. The parish priest, Father Ilya Trushkin, is the dean of the Arzamas district.

The Resurrection Cathedral is the main church of the Arzamas deanery.