The chapel in honor of John of Ustyug was built along with the chapel of Procopius of Ustyug between 1817 and 1820. It is known that a wooden chapel in honor of Procopius was constructed in 1497, and likely at the same time, a chapel in honor of John appeared. In 1737, under Archimandrite Pachomius, the construction of the stone wall of the monastery was completed. Since the church dedicated to the icon of the Vladimir Mother of God, located behind the chapels, served as the Holy Gates of the monastery, both chapels were demolished. In 1814, Archimandrite Pustyn decided to restore the chapels at their original location, and between 1817 and 1820, they were rebuilt. At that time, the walls of the monastery were moved, and the entrance with the chapels of Procopius and John became the new Holy Gates of the monastery.
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