The first wooden church in honor of the Annunciation of the Blessed Virgin Mary was built in Murom in 1192 by Prince Konstantin Svyatoslavich of Murom. In this church, the prince buried his son Mikhail, and later he himself and his second son Feodor were buried here as well. In 1553, the construction of the Annunciation Men's Monastery began on the site of this church, which became the second oldest in Murom. The construction of the monastery's first cathedral is associated with Tsar Ivan IV the Terrible. It was in Murom that he stopped during the Kazan campaign and vowed that if successful, he would build a stone church and establish a monastery 'in the center of the city on the old town site, where the wooden church of the Annunciation was built.' The tsar fulfilled his promise, and in 1553, construction work began. The chronicle reports that the tsar sent stonemasons to Murom, as well as icons, books, bells, and everything necessary for the church from Ryazan. The construction and decoration of the temple lasted about ten years. From 1612 to 1616, the monastery suffered greatly from fires and was plundered by the Poles, but soon its prosperity was restored. According to the inventory of 1637, the Annunciation Church was renewed by the abbot after the devastation. At that time, there was only one stone church in the monastery, 'in the rubble, where there was a fortress, the men's Annunciation Monastery, and in it four churches: the stone Annunciation, St. John the Theologian, St. Gregory the Theologian, and the gate church in honor of Archdeacon Stephen, all wooden.' No other information about the appearance of the monastery cathedral of that time has been found. In 1664, it was almost completely rebuilt with the funds of merchant Tarasiy Borisovich Tsvetnov.

The architecture of the cathedral resembles the Church of the Holy Trinity of 1642 in the nearby Trinity Women's Monastery, which is not surprising, as both monasteries were built at the request of the same benefactor. The influence of Moscow architecture from the mid and late 17th century is also reflected in the appearance of the cathedral. Examples of similar constructions include the Church of the Trinity in Nikitniki, the chapel in honor of the icon of the Mother of God 'Burning Bush' of the Nativity of the Blessed Virgin Mary Church in Putinok, and the Church of St. Nicholas in Pyzhy. In all these churches, the main volume is covered by a vaulted ceiling, decorated with two rows of kokoshniks, while the third row is formed by kokoshniks at the base of the drums of the five domes. The design of the kokoshniks is almost identical, with a semicircular outline and a complex profile. The vault is separated from the main volume by a wide decorative cornice, adorned with various details such as crackers, teeth, and flaps, and complemented by polychrome tiles. The square of the Annunciation Cathedral is modestly decorated and divided into three parts by wide pilasters. From the very beginning of the monastery's history, Tsar Ivan IV the Terrible took care of the church bells, but none of the 16th-century bells have survived. The most famous bell weighed 110 poods and was donated by Prince Mikhail Ivanovich Lvov in 1692, but its fate is unknown. Currently, the selection of bells consists of later examples.