For the first fourteen years of its existence, the Simbirsk Spiritual Seminary did not have its own church, and the seminarians attended the nearby Spaso-Ascension Cathedral. In 1841, a student dining hall was built on the site of the carriage houses in the courtyard. In 1853, under Bishop Theodotius, the dining hall was converted into a church, consecrated in 1854 in honor of Saint Peter, Metropolitan of Moscow. On August 19, 1864, the seminary church, like all the buildings of the seminary, suffered greatly from a fire. During the restoration, it was rebuilt according to a new plan developed by provincial architect A.A. Belousov. On November 8, 1870, the church was consecrated in honor of the Three Saints. Due to its interior decoration and the excellent choir of seminarians, the Three Saints Church was considered the best among the house churches in the city. At the initiative of His Grace Theoktis, in 1879, the Brotherhood of the Three Saints was established at the seminary church to assist poor seminarians. Since 1884, the brotherhood engaged in spiritual and educational activities, helping church-parish schools in the Simbirsk diocese. Its main goal was the spiritual enlightenment of the people, the publication and sale of spiritual literature. In 1896, district branches of the brotherhood opened in all district cities of the province, and it existed until 1917.

The seminary church was closed in 1918, and on November 20 of the same year, its property was transferred to the Ascension Cathedral. For a long time, the building of the seminary church was in neglect. From 1960 to 1996, it housed a sculptural workshop of the artistic fund. In 1996, the building of the church was transferred to the Russian Orthodox Church, but due to the dilapidation of the walls, it was dismantled. Only the bell tower, built in 1893, remained from the former seminary church.

On November 21, 1996, a small wooden church in honor of Archangel Michael was laid before the altar of the former house church of the seminary, and already on February 23, 1997, the first Liturgy was held there. At the end of May 2001, Archbishop Prokl consecrated the site for the construction of a new church and laid the first stone, and in the autumn of 2004, its domes shone over the city.

Since 1998, the construction of a new, more majestic building began on the site of the dismantled church. The project was developed by the chief architect of the city, V.I. Nekrasov.

"A holy place is never empty." First, the church was closed, then it fell into neglect and was destroyed, but now it has been restored and impresses with its beauty. The church serves not only as a place of prayer but also as a house of knowledge. Today, most of its parishioners are teachers from schools and universities in the city, as well as students and graduates of seminaries and academies.

This church is associated with the names of artists P.I. Puzirevsky, S.N. Ogon-Doganovsky, A.A. Plastov, and D.I. Arkhangelsky, as well as the Great Archdeacon Konstantin Rozov, who proclaimed the long-lived at the election of His Holiness Patriarch Tikhon in the Cathedral of Christ the Savior in 1917.

On April 2, 2010, the church in honor of the Three Saints found its voice: the rector of the church, Archpriest Nikolai Kosykh, consecrated the bells. An electronic control system for the bells was installed on the bell tower, allowing them to be rung both manually and with a remote control. This is the first and currently the only such installation in the Simbirsk diocese.