The history of the Nativity parish in Arzamas remains a mystery. It is known that in the early 17th century, in the lower part of the city, by the Shamka River, there stood a church with two altars: one in honor of the Nativity of Christ, the other, the Cathedral of the Most Holy Theotokos. Due to the cramped conditions of the old building, a new church was constructed between 1846 and 1850.

The initiator of the construction was the Arzamas merchant Alexander Mikhailovich Zayashnikov. Starting life as a poor townsman, he became wealthy and amassed a significant fortune. His younger daughter, Evdokia, received a dowry of 50 thousand rubles, but suddenly passed away on August 25, 1845. In memory of his daughter, upon the advice of his spiritual mentor Father Dmitry Raevsky, Zayashnikov decided to spend the dowry on the construction of the church. The church plan was commissioned from architect K.A. Ton, but Alexander Mikhailovich did not live to see its realization, passing away on November 4, 1846. His wife and son-in-law, nobleman Nikolai Yakovlevich Stobeus, continued the construction.

The Church of the Nativity of Christ was soon erected. Architect Mikhail Petrovich Korinfsky Verentsov, known for his work on the Arzamas Resurrection Cathedral, was responsible for the iconostasis. The church received two additional altars: the right one in honor of the Annunciation of the Most Holy Theotokos and the left one in honor of Saint Nicholas the Wonderworker. The consecration took place on October 1, 1850, and the church became a symbol of church construction during the 'golden age' of Arzamas.

In 1939, the church was closed, and on April 7, 1940, it was transferred to a bakery factory. In 1981, the building was handed over to the Gorky special scientific and production workshop for restoration, which continued in 2002 at the initiative of Abbess Sergia from the Serafimo-Diveevo Monastery. Here, one of the three courtyards of the monastery was established.

On August 15, 2010, Archbishop Georgy consecrated the church in honor of the Nativity of Christ. On September 25, he consecrated the chapel in honor of the Annunciation of the Most Holy Theotokos. The last chapel was consecrated on January 17, 2011, in honor of Saint Nicholas and the Holy Martyr Evdokia.