The first church on this site was built in 1103 by the order of Novgorod Prince Mstislav Vladimirovich. The temple was erected in honor of the birth of his firstborn, Mstislav Vsevolodovich, who was baptized with the name Gabriel, in honor of the Archangel Gabriel, one of the two key figures of the Annunciation. This was the second stone building in the city after the St. Sophia Cathedral.

It is believed that the master Peter, known for his works in Novgorod, such as the Nikolodvoriщensky Cathedral, the Cathedral of St. George the Victorious in Yuriev Monastery, and the Cathedral of the Nativity of the Virgin in Antoniev Monastery, constructed the temple.

In 1342-1343, Metropolitan Vasily of Novgorod commissioned the construction of a new church on the site of the dismantled 12th-century building. This church, which existed until 1941, was a large six-pillar three-apsidal temple with a stair tower, typical of Novgorod architecture of the 14th century. The facades likely had three-lobed finishes. The vault and dome collapsed in ancient times and were replaced with wooden ceilings. The church suffered greatly during the Swedish occupation of Novgorod from 1611 to 1617.

In 1797, the temple was extensively rebuilt due to its dilapidated condition, with most of the vaults, arches, and drum dismantled. In 1806, a porch with a small stone bell tower and a chapel of the Meeting was added to the western wall. The floor in the church was wooden. In 1882, the porch and bell tower were reconstructed.

The church functioned until 1930, after which it was closed and not used. During the Great Patriotic War, the church was subjected to German artillery shelling and was almost completely destroyed.

The ruins of the ancient temple were preserved during a large-scale restoration that began in 2016, and in April 2019, they were opened for visitation.