The Assumption Cathedral is built in the Russian national style and features a traditional cross-dome composition typical of such structures. Three semicircular apses adjoin it from the east, and a small bell tower is located on the west side. The church is distinguished by its solemnity and monumentality, which gives it a balance of mass and a moderate use of decor, characteristic of ancient Russian architecture.

The design of the cathedral was developed in 1895 by provincial engineer Alexander Gavrilovich Starzhinsky, who also created projects for many other churches and chapels. In 1905, the consecration of all three altars took place: the main altar, dedicated to the Dormition of the Mother of God, was consecrated on May 1; the left altar, in the name of the Metropolitan of Kiev, Saint Alexius, on May 15; and the right altar, in the name of the Holy Myrrhbearers, on June 19.

In the 1920s, the cathedral was handed over to the Renovationists by the Soviet authorities. On October 25, 1931, after the decision of the Renovationist diocesan administration to merge the communities of the Epiphany, Peter and Paul, and Protection churches, the Assumption Church was granted the status of a cathedral. In 1934, it was closed and turned into a military warehouse. Thanks to numerous petitions from parishioners and the efforts of Bishop Mikhail (Postnikov), who arrived in Penza and secured the return of church property transferred after the closure to the Penza Local History Museum, the church was reopened in March 1945. Bishop Mikhail also moved his cathedra to the cathedral from the Mitrofanov Church.