Originally, the Spaso-Transfiguration Church was wooden and already existed in 1618. Later, around 1670, it was rebuilt in stone, although some sources indicate 1687.

According to the parish books of the late 17th century, the parish of the Church of Andrew the First-Called had 125 households, and the church tribute was significantly higher than that of other churches in Vologda. The clergy included two priests. It is known that from the church of Saint Apostle Andrew the First-Called in the village of Fryazinovo, 3 rubles and 50 kopecks were collected per tithe, which was higher than at other churches.

The parish included the village of Fryazinovo itself, located within the city limits, and nearby villages: Teplenkino, Khorkhorino, Dyakonovo. Thus, the church was unique, combining urban and rural traditions.

Orthodox traditions in the parish were strong. In the annual confession records, priests noted the absence of non-believers and schismatics. In 1733, the spiritual consistory investigated the cases of peasants from the villages of Dyakonovo and Khorkhorino, accused of schism due to the sign of the cross with two fingers and disputes with the priest. The records of 1810 mentioned six people who had not confessed due to schism. Documents also contain information about peasants from the villages of Barankovo, Doronino, and Pogari visiting the church. In 1791, there were 26 people of the spiritual estate and 27 officials with families living in the parish, of which only one family was noble.

In 1922, all the church's valuables were confiscated for the Soviet government: 62 silver items weighing over two poods, pearls, and precious stones weighing over one pound. In January 1930, more than 218 poods of bell metal and 13 bells were thrown down.

On January 31, 1930, the presidium of the Vologda regional committee decided to terminate contracts with eight churches, including the Church of Andrew the First-Called, due to violations by religious communities and the transfer of churches for state needs amid a severe housing crisis in Vologda. Glavsnauk ordered to preserve only the general architectural appearance of the church, while the interior decoration was to be transferred to a museum. The church became a transit point for displaced persons. On its walls and windows, there remained signatures of repression victims, dated 1930-1932, prayers, and children's drawings.

From February 1930, services in the church ceased, and the last rector, Father Nikolai Zamarayev, was transferred to the Bogorodskoye cemetery, where he was arrested in 1937 and died in prison.

After the war, the church housed warehouses for the Vologda oil base. During the Soviet period, no repairs were made, and the building remained without a roof, leading to the destruction of the vaults and damage to the frescoes. All surviving images in the upper church had their eyes gouged out, and the paintings in the lower church did not survive.

In 1990, the church was returned, and services are held in the lower church, where the Andrew and Guriy-Samon-Aviv altars have been consecrated.