The Pechersky Monastery, after being relocated, was initially built of wood, including the Ascension Cathedral. In 1629, Archimandrite Raphael, the monastery's abbot, requested permission from the Patriarch to construct a stone church in the name of the Ascension, noting that materials for construction were already prepared. He repeated the request in 1630, but permission was never granted.

The following year, the archimandrite decided to act independently and invited stonemasons from the Kostroma Ipatiev Monastery, led by Fyodor Oparin, without notifying Moscow. They began the construction of the cathedral's basement, but in 1632, the authorities learned about it, and the stonemasons were sent to state work. Then the monastery created its own construction team led by stonemason Efrem Bosy, which completed the construction of the five-domed Ascension Cathedral with an altar in honor of the Protection of the Holy Virgin by 1640. The church was built according to the designs of architect Antip Konstantinov.

Other buildings of the monastery, such as the tented bell tower, the Assumption Church with the refectory, the gate church of St. Euphemia of Suzdal, the abbot's quarters, and the cells, were also erected according to the projects of this Nizhny Novgorod architect. Antip Konstantinov also participated in the construction of the Archangel Cathedral in the Nizhny Novgorod Kremlin and the Terem Palace, as well as in the restoration of the Assumption Cathedral in the Moscow Kremlin.

A cast-iron commemorative plaque was installed on the Ascension Church, cast in 1858, stating that construction began in October 1631 during the reign of Tsar Mikhail Fyodorovich. A refectory was added to the cathedral, which later became the narthex. A covered porch was made between the north wall of the cathedral and the bell tower, and a brick porch was added on the south side, which was demolished in the 1970s during restoration.

The architectural style of the Ascension Cathedral traces back to the Assumption Cathedral of the Moscow Kremlin. The cathedral is four-pillar, five-domed, standing on a high basement, which was used as a vegetable storage during Soviet times, while the upper church served as a carpentry workshop. The smaller domes of the cathedral vary in size, two of which illuminated the altars in the choirs and were built more massive. The refectory part of the cathedral, transformed into a narthex, had a western entrance and a ceremonial porch with clay voice openings in the walls. Until the mid-18th century, the roof of the cathedral was made of shingles, and from 1759 to 1766, it was covered with iron, and in 1783 it was made four-pitched. The roof has now been restored.

In 1924, the monastery was closed by the decision of the NKVD, and soon the Holy Ascension Cathedral was also closed. In 1971, craftsmen partially restored the ancient appearance of the cathedral. In the 2000s, modern craftsmen, such as Vladimir Ivanovich Nekrasov and Dmitry Nikolaevich Mishchenko, worked on the restoration of the church. In 2004, the refectory was painted by icon painter Oleg Romanovich Shurkus. The consecration of the main church of the Pechersky Monastery took place in 2000 on the feast of the Ascension of the Lord.