On February 15, 1997, on the day of the Meeting of the Lord, a site was consecrated for the construction of the main church of the Blagoveshchensk Diocese, the cathedral, at the intersection of Komsomolskaya Street and Relyonok Lane, and a cross was erected. In 1998, archaeological excavations were conducted at this site, during which household items and burials were discovered: the first priest of the Amur region, Archpriest Alexander Sizov, military doctor Mikhail Davydov, and unknown male and female remains. The remains were reburied in 2002 near the apse of the newly built church; prior to that, they were kept in the regional local history museum. The cathedral site has historical significance. In 1857, here, on a hill, Cossack pioneers built the first house of the city and St. Nicholas Church, and in 1879, the first stone church of the Protection of the Mother of God appeared nearby. The new Blagoveshchensk Cathedral was built based on this Protection Church. Archaeologists also found an old brick base of a flagpole, where a steel mast with the Russian flag was installed in memory of the flag of the Russian Empire, raised by the Governor-General of Eastern Siberia N. N. Muravyov-Amursky and Archbishop of Kamchatka Innocent (Veniaminov) in honor of the annexation of the Far East to Russia. In 2009, a monument was erected here in their honor.

The three-altar cathedral has a cross-shaped plan. The main altar is dedicated to the Annunciation of the Blessed Virgin Mary, while the two chapels are dedicated to Saint Nicholas the Wonderworker and Saint Innocent (Veniaminov). The church is adorned with seven gilded domes, and the eighth dome crowns the bell tower. The largest bell weighs 1280 kg and has a diameter of 1.2 m. The height of the main dome to the base of the cross is 38.85 m, and the height of the bell tower is 32.5 m. The church accommodates 540 people. The basement houses a baptistery with a pool for adult baptisms.

In 2012, the cathedral was renovated and adorned with new icons, and the Albazin Icon of the Mother of God was moved to a separate chapel. In 2015, a new glazed vestibule was added to the entrance of the church to increase its capacity.