The history of the church begins with the creation of a cemetery. From 1760 to 1770, epidemics severely devastated Russia. One of the reasons for the constant illnesses was believed to be cemeteries within cities, and in 1772, Catherine the Great ordered the establishment of new cemeteries outside the cities. In 1782, surveyor Neelov described the Bogoroditskoye cemetery as located along the Vologda River, upstream on the left side, opposite the old cemetery of St. Nicholas the Wonderworker, which is in Glinki, three hundred fathoms from the last line of the rampart. Initially, funerals took place in the Glinkov church, so the cemetery was called the Zaglinkov Nikolayevsky. Burials began here in 1781.

The first stone church was built no later than 1790 and was named the Nativity of the Blessed Virgin Mary at the Glinkov cemetery. Later, the cemetery became the main one in the city, but the church turned out to be too small for the residents of Vologda. The construction of a new church, which still stands today, began in 1832 under the guidance of church elder Alexander Ivanovich Popov-Testov. The church was built and consecrated in 1836. It was made of stone, with a bell tower located in the dome above the cold church, two stories high and sturdy. In the early 20th century, at the initiative of elder Nikolai Kubryakov, the refectory part of the church was extended and the entrance to the second floor was remodeled, giving the church a modern outline.

In the second half of the 1930s, the authorities sought to close the church. In 1937, the cemetery was closed for burials, and in 1938, the upper 'renewal' church closed due to a lack of parishioners. The building housed the NKVD archive. In 1937, the NKVD arrested all Vologda priests in one night. Only Father Alexander Belyaev, who was out of town, and Nikolai Dobryakov, who suffered from thrombophlebitis in his legs, escaped arrest. For almost a year, overcoming pain, he continued to serve in the church, which became a true feat. In 1939, during a service, he had an attack and was taken to the hospital, where he passed away. The authorities again raised the issue of closing the lower church, but the Orthodox community held firm. Three months later, a new priest, Anatoly Gorodetsky, was found.

During the war and in the early post-war years, many returned to the Church. The authorities were forced to reopen a number of churches. The question of opening the Resurrection Cathedral arose, especially relevant in 1947, on the eve of the city's 800th anniversary. At that time, they were looking for a 'host' for the cathedral: first the regional museum, then a club, and finally an art gallery. However, officials were forced to compromise and instead of the Resurrection Cathedral returned the upper church of the Bogoroditskaya church to the believers, which became the cathedral. On August 18, 1992, His Holiness Patriarch of Moscow and All Russia Alexy II celebrated the Divine Liturgy at the Nativity of the Blessed Virgin Mary Cathedral.