On February 2, 1677, by the order of Patriarch Joakim, the construction of the stone Assumption Cathedral began in the monastery, overseen by Abbot Euphemius. The Church of the Assumption of the Blessed Virgin Mary in the Dudino Monastery was built with an altar dedicated to St. Nicholas the Wonderworker. By 1764, during the secularization of church lands by Catherine II, the monastery, which had only 6 monks remaining, was closed. The Assumption Church became the parish church of the village of Pod'yablonnoe in the Gorbatov district nearby. By the early 19th century, the monastery ensemble was almost destroyed, but the parishioners supported the Assumption Church. In the 1820s, with funds from the parish, its roof was repaired, replacing the wooden one with an iron one, and the refectory was completely rebuilt, reinforcing its vaults with two columns.

In the late 19th century, the bell tower of the Dudino Monastery attracted the attention of architect L.V. Dal with its archaic architecture. He made a watercolor of it and measurements, which were later published by the Imperial Archaeological Commission. In the early 20th century, the monastery ensemble began to be perceived as an ancient monument worthy of preservation. From 1910 to 1912, under the guidance of Nizhny Novgorod architect Leonid Dmitrievich Agafonov, repair and restoration work was carried out on the Assumption Cathedral, and its ancient iconostasis was restored.

The two-altar stone Assumption Church is traditional in its volumetric-spatial solution: the two-tiered square of the main volume is covered by a vault, with a three-apse altar to the east, and to the west, an elongated refectory under a gabled roof adjoins it. The flanks of the square are highlighted by pilasters and topped with semicircular zakomaras, with a profiled cornice running along the upper part. The rectangular windows lack decorative framing. The conciseness of the architectural appearance and the massive buttresses create a sense of the church's monolithic nature.