On the site of the wooden church of the Annunciation of the Blessed Virgin Mary, which, according to church tradition, was built by Saint Prince Constantine Svyatoslavich, the younger son of the Chernigov Prince Svyatoslav Yaroslavich and the grandson of Yaroslav the Wise, a new structure arose. Some sources also consider him the grandson of Yaroslav Svyatoslavich of Ryazan.

According to church legend, the local inhabitants remained pagans for a long time, worshipping the forces of nature. Upon learning this, Prince Constantine asked his father for the land of Murom to convert the townspeople to Christianity. He was assisted by his sons Mikhail and Fyodor. The Murom pagans resisted and even killed the younger son Mikhail. However, upon seeing a miraculous sign from the icon of the Mother of God, brought from Byzantium and named the Murom Icon, they repented and accepted baptism in Lake Kstovo. In this temple, Saint Bishop Basil prayed.

In 1547, Prince Constantine and his sons Mikhail and Fyodor were canonized. The monastery was founded in 1553 by Ivan the Terrible after his visit to Murom in 1552. Since 1555, the relics of Prince Constantine were kept in the Annunciation Cathedral. In 1616, the monastery was destroyed by the Poles, but in the 17th century it was gradually restored. In 1664, the Murom merchant Tarasiy Tsvetnov rebuilt the Annunciation Cathedral and installed a clock on the bell tower. In 1791, the Murom Spiritual School was opened on the monastery grounds. After the fire of 1792, the stone buildings and shrines survived, but the school was moved to another house and closed in 1800.

During the Patriotic War of 1812, the Iver and Vladimir Icons of the Mother of God were kept in the monastery. In 1866, the monastery received a second class, and in 1867 and 1882, it was managed by the Bishops of Murom. The monastery was closed in 1919, but the brotherhood continued to serve in the cathedral. In 1923, the relics of Princes Constantine, Mikhail, and Fyodor were exhumed and transferred to a museum, where they remained until 1989. In 1940, the cathedral was closed, but two years later it became a parish church. In 1946, Hieromonk Pimen Izvekov, the future Patriarch of Moscow and all Rus, served here. In 1991, the Holy Synod renewed monastic life in the monastery. In the crypt of the cathedral rest the relics of Saint Basil of Murom and the Venerable Julian Kochukov.

The necropolis of the monastery contains the graves of notable residents of Murom and clergy, including the abbot of the monastery, Archimandrite Alexiy Polysadov, the great-grandfather of poet Andrei Voznesensky.

The main church of the monastery is the Annunciation Cathedral, the construction of which began in the 16th century, with reconstruction occurring in the 1660s. The exterior decoration of the cathedral is an example of ornamental style. The Annunciation Cathedral is the only building that survived the devastation of the monastery during the Time of Troubles. A tented bell tower is attached to the cathedral, and the St. Stephen Church dates back to 1716. In 1811, a monastery fence with towers was built.