The history of the construction of the church in honor of the righteous St. John of Kronstadt in Ryazan began on November 18, 2008, when the city's residents requested to consider the possibility of building a church, a dependency of the Spaso-Preobrazhensky Monastery, in the city park near the Poletayev monument. On May 12, 2009, Archbishop Pavel of Ryazan and Kasimov consecrated the land for the construction of the dependency in honor of St. John of Kronstadt. For a long time, the possibility of building at this site was discussed. Thanks to the efforts of Archbishop Pavel and the city administration, a positive decision was made. The location was chosen well, as it is in the center of the city, at the intersection of several densely populated neighborhoods and at the crossroads of highways in one of the highest points of the city. On June 16, 2009, preparations for the foundation of the church began, and on July 20, 2009, the foundation was poured. The consecration of the cornerstone took place on November 27, 2009.

The church complex will consist of four floors: a basement with a lower church, the first above-ground floor with a spiritual and educational center, the second floor with a brotherhood building, and the third floor with the church in honor of St. John of Kronstadt. By May 2010, the construction of the first above-ground floor was completed, and by November 17, 2010, two above-ground floors were fully erected. A heating point was installed on the adjacent territory. One of the resolved tasks was placing an order for the production of complex architectural details from archstone in Moscow. Facing bricks were delivered from Ukraine and Rostov-on-Don. Representatives of the Spaso-Preobrazhensky Monastery, led by Abbot Ignaty Deputatov, visited the St. John's Stavropegial Convent in St. Petersburg. Architect Father Konstantin Kamyshanov conducted the necessary measurements of the Cathedral of the Twelve Apostles. Plans from the BTI were sent from St. Petersburg to Ryazan. A distinctive feature of the Ryazan church is the relocation of the bell tower to the central axis, which is justified since the church is a separate building. The architectural details of the church demonstrate the unity of religious and aesthetic aspects of Orthodox art. The internal forms of the church, in elegance and beauty, do not yield to the external ones, which testifies to the preservation of the traditions of church art and architecture.