In 1525, a wooden church was built to serve the residents of the monastery settlement. Here, they were baptized, married, and given funeral rites. In the second half of the 16th century, a new brick church was erected in place of the wooden one, standing about 35 meters tall. It featured a tented roof, similar to the Church of Martyr Nikita in the village of Yelizarovo and the Church of the Nativity of Christ in the village of Besedy.
By the late 17th century, as the congregation grew, a small five-domed side chapel dedicated to St. Nicholas the Wonderworker was built next to the brick tented church. This ensemble existed until 1812.
During the French occupation of Moscow, the Church of the Beheading of John the Baptist with the side chapel of St. Nicholas was one of the few churches in Moscow destroyed by Napoleon's orders. In 1816, a new church was built on another site for the settlement’s residents near Maiden’s Field, dedicated to the Fathers of the Seventh Ecumenical Council. This dedication commemorated the day Napoleon’s forces left Moscow. In the 1930s, this church was also destroyed, but by the atheist authorities of the Soviet regime.
The decision to reconstruct the church was made by the Chairman of the Government of the Russian Federation and President-elect Vladimir Putin, together with His Holiness Patriarch Kirill of Moscow and All Russia, on May 6, 2012. This occurred during the ceremony of returning the Iveron Icon of the Mother of God from the State Historical Museum to Novodevichy Convent.
Before construction began, archaeological excavations were conducted on the chosen site by the Institute of Archaeology of the Russian Academy of Sciences in 2013 and 2015, as part of a program by the Department of Cultural Heritage of Moscow.