The Church of the Nativity of the Blessed Virgin Mary, built of stone in 1767, replaced a wooden structure from 1564. It was renovated in 1859, receiving marble walls and ceilings. In the 1760s, the old Church of the Nativity was dismantled due to its dilapidated state. According to documents from 1763, a five-domed stone church with a refectory was erected in its place, with alabaster plaster covering the walls and ceilings, and decorations made of stucco and painted. The church had storerooms, a porch with a gallery, and a stone staircase, as well as a wooden platform with railings and stairs to the tombs of the benefactors. The church existed for about a hundred years but was replaced by a new one between 1860 and 1863, which also did not survive. It was destroyed in 1932 when the Bolsheviks closed the Ipatiev Monastery.

In 2008, a decision was made to recreate the Church of the Nativity of the Blessed Virgin Mary in the Ipatiev Monastery on the site of the destroyed one. The initiative was led by the President of Russia, D.A. Medvedev, and the blessing was given by Patriarch Alexy II. The opening and consecration of the new church were timed to the 400th anniversary of the restoration of Russian statehood. The monastery needed a spacious church for daily services to preserve the unique frescoes and icons of the Trinity Cathedral.

The reconstruction of the church was completed in 2013, as planned. It was built in the style of the second half of the 19th century on the site of the demolished building, southwest of the Trinity Cathedral.