One of the oldest and most interesting architectural monuments of Simbirsk was destroyed in the 1930s. This church, the second temple of the monastery with the same dedication, replaced a wooden structure built in 1697 and consecrated on January 5 of the following year. The new stone church in the Naryshkin Baroque style was built between 1720 and 1724. The bell tower, according to some sources, appeared later but is stylistically and structurally part of the building. It is possible that the entire western volume dates back to the 1730s. At that time, a decree by Peter I was in effect, prohibiting stone construction outside of St. Petersburg, which was lifted for the provinces only in 1729. Stone buildings on the Middle and Lower Volga were rarely constructed during this period and only with special permission. An example is the Peter and Paul Cathedral in Kazan, built by merchant Mikhlyaev, a close associate of the tsar. Architecturally, the church in Simbirsk was similar to Kazan buildings, and it is possible that it was built by a Kazan craft guild, as Kazan was a significant construction center before the ban, quickly adopting metropolitan architectural trends. However, the connection of the church's builder, clerk Pyotr Ivanovich Muromtsev, with Peter I remains unclear.

The church was completed in 1724, with the right chapel of the Protection of the Blessed Virgin Mary, corresponding to the name of the monastery, being consecrated first. Later, the main chapel of the Annunciation of the Blessed Virgin Mary and the left chapel in honor of the Four Holy Hierarchs of Moscow were consecrated. In 1737, the chapel of All Saints was consecrated in the second tier of the bell tower, which was repaired in 1846 at the expense of E.A. Stolypin and re-consecrated in honor of Alexander Nevsky. It is difficult to say exactly when the church acquired its final appearance, known from archival photographs. In them, it is presented as a three-part volume, reminiscent of churches from the late 17th to early 18th centuries, but differing from the usual 'three-domed' composition: the central volume is narrower than the eastern and western ones. Only the central and eastern volumes have Naryshkin decor, confirming that the western volume is a two-story narthex. The late dating of this volume is supported by the classicist decor, which is also present on the lowered volumes to the north and south. These extensions can be attributed to repairs in 1809 or to 1846, when the chapel under the bell tower was corrected. It is possible that other works were also carried out at that time, which can be clarified by studying the archives. The central square is two-light, on which four decreasing octagons are installed, including two tiers of ringing, a church type 'under the bells', completed with a drum and a dome. The eastern volume is wider but lower, has a simple four-pitched roof, and is topped with one dome, with a semi-circular apse adjoining from the east.