The Annunciation Cathedral was built in 1810 by Lieutenant Fyodor Ivanovich and Yevdokiya Avraamovna Rakhmanov in the style of Russian classicism. This church is known for having served the now-canonized saint, confessor Raphael (Sheichenko).

The stone church with a bell tower and fence was constructed in 1810 by the same Rakhmanovs. According to archival data, a wooden church existed in Kozelsk since 1709. The bell tower was added later: according to some sources, in 1825, and according to others, in 1832. In 1871, the refectory part of the church was expanded and improved thanks to the efforts of parishioners and the church elder, merchant Venedikt Petrovich Lavrentyev.

The merchant class played a significant role in the life of the church. Some merchant families bequeathed percentages from bank accounts for the maintenance of church servants and the commemoration of their relatives. In 1895, the church received a new bell and updated decorations thanks to donations from the Tsyplakov family.

The Vyrsky School, founded by Deacon Fyodor Vyrsky and his daughter Anna, became an important phenomenon in public education. Initially, it was a private school where children learned literacy at the deacon's house starting in 1833. In 1860, Vyrsky opened a second parish school in the city. By 1860, 250 children were studying at the school, including up to 120 girls. In 1861, the famous educator K.D. Ushinsky visited the school. The Vyrskys also worked at the Kozelsk Diocesan School and the Annunciation Church Parish School.

Fyodor Vyrsky's daughter, Alexandra Fyodorovna Vyrskaya, continued her father's work and was awarded a gold medal in 1902 for over 50 years of pedagogical activity.

The church was closed and looted in 1937. Nearby was a cemetery for clergy and notable people of Kozelsk, but after 1937, the gravestones were destroyed.

During the war (1941-1942), services were held in the partially destroyed church by Archpriest Stefan Akulin. The church became the only functioning one in Kozelsk. Here served the venerable Raphael (Sheichenko), who improved the church by erecting iconostases and restoring the bell tower. From 1944 to 1948, the abbot Nikon (Vorobyov) served in the church.

Near the church is buried the blessed silent monk Tit, who lived in a lodge by the church in the first half of the 19th century, known for his feats of silence and prayer.

Currently, all-night vigils and liturgies are regularly held in the church for all twelve major feasts and great holidays, as well as on Saturdays and Sundays, for feast days and particularly revered celebrations. On Friday evenings, matins is performed with the reading of the Akathist to the Mother of God.