The Assumption Church, adorned with icons and other beauties, existed for a short time. According to tradition, it burned down as a result of a severe fire that occurred between 1462 and 1497. In 1462, Pachomius the Serb, the author of the life of Cyril, still saw it.

The Assumption Cathedral, built in 1497, became the first stone temple of the Kirillo-Belozersky Monastery and the third in the Russian North. Before it, there were two wooden Assumption churches. In 1641, the cathedral was painted by the icon painter Lyubim Ageev, who, in 1643, after returning from Kirillov, worked on the painting of the Assumption Cathedral of the Moscow Kremlin. Due to a lack of local builders and craftsmen, the monastery sought help from Rostov Veliky, the center of its diocese. According to chronicles, in 1497, Rostov masters, 20 stonemasons and builders led by Prokhor of Rostov arrived in Kirillov, who erected the stone cathedral in one summer season.

The chronicles referred to the new Assumption Cathedral as the 'great church.' For its time, it was indeed significant, surpassing in size many buildings in Moscow and other cities. Even today, despite subsequent changes, the building retains a majestic and solemn appearance. Its compact cubic volume with three wide semicircular apses is topped with a powerful dome. This type of church was common in Northeast Russia in the second half of the 15th century, during the formation of all-Russian architecture under the leadership of Moscow. However, it is characterized by massiveness and simplicity. Devoid of a basement and originally free from extensions, the cathedral seems to grow out of the ground, impressing with its monumentality and coherence of forms.

In 2013-2014, extensive restoration work was carried out on the Assumption Cathedral.