The church was established in the academic hall, where public examinations were previously held, and was consecrated on February 12, 1870. Initially, the academic church was small, and its altar faced south, which contradicted the 91st rule of St. Basil the Great, according to which during prayer one should look east, striving towards the ancient paradise that God planted in Eden in the east.

Over time, rectors in the rank of bishop began to appear at the Moscow Academy, and the academic worship became more solemn. There arose a need to expand the church, and in 1892, when Archimandrite Anthony was the rector, the church was increased more than twice, and the altar was turned to the east. The church in its new form was consecrated on September 20, 1892, shortly before the celebration of the 500th anniversary of the repose of St. Sergius.

However, even in its updated form, the church stood for almost as long as the original. It was low and dark, lacking architectural merits. In the summer of 1913, a new reinforced concrete vault was constructed over the church, making it twice as high. On November 16, 1913, services began in the reconstructed church, but it lacked the beauty of an Orthodox church that corresponded to the new height of the iconostasis and wall paintings. According to the holy fathers of the Seventh Ecumenical Council, the church's beauty, consisting of pictorial images, serves to assure the true embodiment of the Word of God and is beneficial, as those gazing at the sacred images are inspired by memories and love for the prototypes. It was especially important to give the church the appearance of a true Orthodox church in anticipation of the 100th anniversary of the academy, which was planned to be celebrated solemnly. However, the lack of funds hindered the process. From the very beginning of the reconstruction of the vault, appeals were made to private benefactors, and then to all former students of the academy for donations to the church for the anniversary. Archpriest A.V. Gorsky, who arranged the church, also appealed to close individuals of the academy for assistance in beautifying the church. The gifts of these old students still adorn the academic church.

In early 1914, about a thousand appeals were sent out: "In 1914, the Moscow Spiritual Academy will celebrate its 100th anniversary. One of the urgent needs is to bring the academic church into decent condition. The reconstructed church needs utensils, there is no iconostasis corresponding to the new height, and the sacristy is dilapidated. The memory of former students of the academy lives in the church, where all who taught and learned, governed and served are commemorated. This circumstance gives us the courage to appeal to all close individuals of the academy to remember the church and donate funds to give it a worthy appearance."

Not all students of the academy received the appeal, as the academy does not know where its graduates live and work. Nevertheless, donations began to arrive. The academy expresses deep gratitude to all donors.

In June 1914, immediately after the end of classes, the painting of the vault and walls of the church began. The altar painting was undertaken by architect Sergey Semyonovich Makarov, while the vault and walls were painted by Petrograd artist N.A. Protopopov, a graduate of the Kazan Spiritual Academy. The church is painted in the new Kyiv style, predominantly in the style of Vasnetsov, with scenes from the Vladimir Kyiv Cathedral. The vault features paintings by Vasnetsov: "The Word of God," "Crucifixion," and "God the Father," while in the choir, "The Last Judgment." On the sides of the vault, "The Precursor of Paradise," and in the corners, the evangelists with their symbols. The dome is decorated with Byzantine ornamentation and symbols of the days of creation, and at the top, "The Savior with the Gospel." Above the iconostasis window, three Angels. The walls are adorned with images of saints. Thanks to the artist's talent, the painting is characterized by unity and makes a strong impression. In the altar on the ceiling, "The Protection of the Holy Virgin," on the wall, "The Mystery of the Eucharist," and on the sides, "The Nativity of Christ," "The Burial," and images of the Apostle James, Saints John Chrysostom, Basil the Great, Gregory the Dialogist, and others.

The iconostasis now consists of three tiers. In the upper tier above the royal gates, the icon of "The Protection of the Mother of God," which descends to the ambo during some services.