The Assumption Church, the oldest monument of temple architecture, is located outside the Kremlin, on the landing, a bit away from the center. Its construction was completed by 1553. Remarkably, the "porydnaya," enclosed by Rostov masters with the clergy and parishioners of the wooden predecessor of the Assumption Church, has survived. The document states: "I, Goryain Grigoriev son of Tsarev, and I, Tretyak Borisov son of Rostovka, have agreed to build a stone church of the Assumption of the Most Holy Theotokos on Belozersk. And to build the church, as in the Kirillov Monastery, the church of the Assumption of the Most Holy Theotokos, with smooth work, and in the wall we are to make a place for large and small bells, and to erect a chapel on the church. And we shall take for that work for the wall builders and for craftsmanship ninety rubles."

There is a legend that in 1613 the Assumption Church was ravaged and desecrated by the Poles, who kept horses in it and kindled fire. Traces of this barbarism are visible in the form of a horseshoe imprint on the icon of the Theotokos of Tikhvin, on the right hand, which is now painted over and almost indistinguishable, as well as in the form of a charred beam in the altar, protruding from the wall under the ceiling. The watch book of 1617-1618 describes the iconostasis of the church at that time in detail: "The Church of the Assumption of the Most Pure Theotokos and the chapel of Metropolitan Alexei, another chapel above the Entry into Jerusalem of our Lord Jesus Christ with five tops, stone. And in the church on the table of Deesis, there are 12 images on gold, on another table 20 images, and on them are written the feasts; on the table 18 images, and on them are written the prophets; the royal doors and columns, and the canopies are in gold."

In the 18th century, the original iconostasis was replaced with a new baroque one, but the masters preserved the simplicity and strictness of the ancient church. This iconostasis, unlike that of the Spaso-Transfiguration Cathedral, belongs to the traditional type of Russian iconostases and includes 60 icons. Judging by the individual cleared icons, they were created by a craft group of local masters who, in those years, painted icons for the Church of John Climacus in the Kirillo-Belozersky Monastery. A significant part of the old icons, contemporaries of the Assumption Church, "transitioned" to the new iconostasis and have survived to this day. Unfortunately, in 2004, the iconostasis lost its unique royal gates, which were stolen and have not yet been found. In 1784, next to the cold Assumption Church, a warm Epiphany Church was built, executed in a somewhat archaized style. A remarkable bell, which had long stood on the porch of the Assumption Church, is now raised to its bell tower.