It is believed that the Annunciation Monastery was founded almost simultaneously with Nizhny Novgorod and was devastated in 1229 by the Mordovian prince Purgas. The Laurentian Chronicle mentions the monastery in 1229, which is the first reliable mention of the monastery in written sources.

There is a version that the monastery was founded in 1221 during the establishment of Nizhny Novgorod by Grand Prince Yuri Vsevolodovich and Bishop Simon. This idea emerged in the 19th century. Chronicles report that under Yuri Vsevolodovich, the Monastery of the Holy Mother of God was founded near Nizhny Novgorod. Archimandrite Macarius suggested that this was the Annunciation Monastery, and this opinion became popular, although it is not supported by facts.

Historian A. A. Kuznetsov argues that the identification of the Mother of God Monastery with the Annunciation Monastery has no scientific basis. The similarity lies only in the names, and mentions of the Annunciation Monastery appear only in the second half of the 14th century. In his opinion, the connection between the monasteries is based solely on the coincidence of the name of the Mother of God.

The Mother of God Monastery could have been associated with other monasteries, such as the Assumption, Praise, Nativity, Protection, or the Entry into the Temple of the Mother of God. Confusion in historiography arose in the 19th century when local historian N. I. Kramtsovsky wrote that the Annunciation Monastery was the same as the Mother of God Monastery, devastated by Purgas in 1229. The authority of Stroeva, a companion of Karamzin, was high, which influenced the creation of the monastery's history from 1229 to 1357, when it was allegedly restored by Metropolitan Alexius.

The monastery performed defensive and missionary functions. In the 14th century, the monasteries of the Nizhny Novgorod-Suzdal principality actively participated in the development of lands. A significant part of the territory was deserted and was developed by monks and peasants. From the late 14th century, the monastery began to develop crafts.

In 1393, Prince Boris Konstantinovich granted the monastery crafts along the Sura River and lakes. In 1399, boyar Savva Syuzev bequeathed wasteland in the Kurmysh district to the monastery. In 1416-1417, wasteland on the Platin Vrag was transferred to the monastery. In 1438, Prince Vasily Vasilyevich transferred the village of Yelenskoye and the village of Zaborovskoye to the monastery, and in 1442, Prince Daniil Borisovich, the village of Migino. In 1554, the monastery received the village of Gnilitsa.

After the revolution, the monastery was closed and devastated. In 1948 and 2005, a planetarium was located in the Alexiev Church. The revival of the monastery began in 1993 with the opening of a spiritual school, which later became a seminary. The first rector was hieromonk Kirill. In 2007, a porcelain iconostasis was installed in the church of St. Alexius, the first in Nizhny Novgorod.

On April 7, 2009, the icons of the patriarchal row of the iconostasis of the Annunciation Cathedral were consecrated. Since 2010, parishioners have been helping to restore the Church of John the Baptist in the village of Prudishchi. On May 7, 2011, Archbishop Georgy consecrated the church of Sergius of Radonezh. On August 23, 2013, a bust monument to Alexander III was opened on the territory of the monastery.