The construction of the monastery took place in 1697 and 1700 under the guidance of P.I. Muromtsev. The first church, consecrated in honor of the Annunciation of the Most Holy Theotokos, was wooden, and the monastery was originally called the Annunciation Monastery. In 1720 and 1724, Muromtsev built a stone Annunciation church on its site with two chapels: the left one dedicated to the four Moscow saints, Peter, Alexius, Jonah, and Philip, and the right one in the name of the Protection of the Most Holy Theotokos. The latter was consecrated first, which gave the church and monastery a second name, Pokrovsky. In 1724, monks were transferred here from the abolished Assumption Monastery in Podgorye, and in 1764, monks from the Solovetsky Monastery. Later, Muromtsev added a stone bell tower to the church with a chapel in honor of All Saints, consecrated in 1737. In 1846, with funds from E.A. Stolypin, this chapel was renovated and renamed in honor of Saint Alexander Nevsky.

By 1764, the monastery was surrounded by a stone fence measuring 70 by 63 fathoms and slightly over 3 arshins high. In 1780, there was one stone church in the monastery, while the number of other buildings changed over the years. A garden surrounded the church, and on the southern side was a cemetery for the monks. Between the western wall of the fence and the Sviyaga River were the monastery gardens.

Since the establishment of the independent Simbirsk diocese in 1832, the Pokrovsky Monastery became the Archierial House, and its staff was transferred to the Syzran Resurrection Monastery. In 1785 and 1787, a wooden abbot's house was built on a stone foundation, where Simbirsk bishops lived in 1832 and 1844. During this period, the spiritual consistory was located in the monastery, and in 1724, a charity house for the disabled, which requires verification, was established. It is possible that retired soldiers were supported by the monastery but lived outside its bounds, and a charity house for them existed in the 1750s and 1760s. The first bishop, Anatoly, arranged a church in the name of Saint Mitrophan, the Wonderworker of Voronezh, in this house in 1836. In 1844, a new Archierial House was acquired on Vents, but the monastery continued to remain a dependency of the Archierial House.

The monastery was closed on May 3, 1932, and its buildings were planned to be used for the cultural and domestic needs of the city's workers. At the request of the workers, the monastery church was supposed to be used as a warehouse for agricultural machinery, but according to locals, services continued in the church even in 1934. The monastery was destroyed by 1934, and only three buildings and a small part of the monastery wall on Ulyanovsk Street have survived from the entire complex.