The church of St. Cyril of Belozersk was first built in 1585-1587 over the grave of the monastery's founder. Its construction was linked to the dissatisfaction expressed by Ivan IV in a letter from 1573 to the abbot Kozma and the brethren of the Kirillo-Belozersky Monastery: "But you have built a church over Vorotynsk! Only over Vorotynsk a church, but over the miracle worker there is none, Vorotynsk is in the church, but the miracle worker is behind the church." However, even after receiving this letter, the monastery elders did not rush to build a stone church and only laid its foundation twelve years later, after the death of Ivan the Terrible. The church built over the relics of St. Cyril in the 16th century was the only stone structure that has not survived to this day. It stood for about 200 years and was dismantled due to dilapidation.

The Church of Cyril was rebuilt in 1781-1784. The new building is designed in the late baroque style. From the outside, it appears to be a tall church with an octagonal base and a lower wide refectory, but this is not the case inside. Externally, the church is divided into three tiers: the altar was located in the lower tier, while the two upper tiers housed the monastery's sacristy. The church was situated in the western part and represented a high two-light hall without a light drum. In the northern wall, in a deep arched niche, was the reliquary of St. Cyril.

In 1828, the church was converted into a warm one, and at that time a suspended ceiling was made, the lower windows were enlarged, and the trim was removed. These changes led to the loss of the interior decoration, including the rich iconostasis and precious items.

Today, the church has been restored. In 1997, the temple of St. Cyril of Belozersk was transferred to the Orthodox religious organization "Kirillo-Belozersky Male Diocesan Monastery" for conducting services. In 2010, the museum transferred 29 copies of icons from the iconostasis of the Assumption Cathedral to the monastery, which are now placed in the iconostasis of the church of St. Cyril.