The building was built in 1900-1902 by the architect Nikonov. The lower Church was consecrated in honor of St. John of Rila (Rylskiy), the heavenly patron of the Dear Father, and the upper Cathedral-in honor of the Twelve Apostles. The abbess of the monastery was the spiritual daughter of Fr. John, hegumeness Angelina (Sergieva) (1867-1927).

From the very beginning, father John had been especially concerned about the improvement of the new monastery. Even during the life of the Priest, his works and prayers, the monastery had reached its peak. The monastery attracted worshippers with its statutory services and the touching singing of the sisters. Fr.John liked to call himself "the Builder of the John’s monastery by the grace of God". Here were his chambers, where he stayed during a visit to the Northern capital. Here was also built a temple-tomb, in which, according to the will of the Father, he was buried on December 22, 1908. The tomb was consecrated in the name of the prophet Elijah and Queen Theodora, the heavenly patrons of Fr. John.

By 1917, the monastery had 350 sisters. The sisters did almost everything they needed themselves. The monastery had its own subsidiary farm, workshops, and hospital. Charitable assistance was provided to those in need, and there was a shelter for orphans. During World War I, the monastery opened an infirmary for wounded soldiers and officers.

After the arrival of the new government, the monastery was closed in 1923, all the property was taken out and looted, and the building was transferred to the management of more than 20 different organizations. In the following years, almost all of the sisters were arrested and sent to prisons and camps.

In 1989, the monastery began to return to the Russian Orthodox Church. In the 70 years that have passed since the monastery was closed, the building has fallen into a severe decline. The temples and all the rooms were rebuilt. It took several years of intensive repair and restoration work to return the monastery to its original appearance.

Simultaneously with the restoration of the walls, the revival of monastic life began. After the consecration of the upper Church by his ever-Memorable Patriarch Alexy II of Moscow and All Russia on July 13, 1991, services are held daily at the monastery. Gradually, the work of monastic workshops is being adjusted. In the Church-tomb of St. John of Kronstadt a small Museum dedicated to him and the history of the monastery was created. The monastery has a free Sunday school. In 1992, the monastery was granted the status of a stauropegion and since then it has been under the direct authority of his Holiness the Patriarch of Moscow and All Russia.