The construction of a new summer church next to the ancient Christ-Redeemer Cathedral was prompted by its small size and dilapidation, as well as the cramped and stuffy conditions, especially noticeable during winter services. In 1677, Metropolitan Joseph of Ryazan appealed to Tsar Fyodor III Alexeyevich for permission to build a more spacious cathedral nearby, on the site of the gunpowder chamber. In 1679, by the tsar's decree, the gunpowder chamber was dismantled. In March 1684, "mason apprentice Fyodor Sharitin and his companions" signed a contract with Metropolitan Pavel Moravsky to construct a new cathedral for 1250 rubles and additional supplies. The work was to begin on the 15th and be completed within three years. In 1692, Metropolitan Avraamy joyfully informed the Patriarch and Tsars Ivan and Peter Alexeyevich that the construction of the cathedral was completed, the vaults were being raised, and the necks for the domes were half-finished. However, on the night of April 18, 1692, the cathedral collapsed due to miscalculations or weak soil, also destroying the church of Varlaam Khutynsky in the Spassky Monastery.

In January 1693, Metropolitan Avraamy organized a new competition for the construction of the cathedral, and the foundation of the current Assumption Cathedral was laid. The contract was awarded to master Yakov Grigoriev Bukhvostov. Work began on May 18, 1693, and by the end of 1699, the cathedral was covered and had five domes. The workshop of carver Sergey Khristoforov created a seven-tiered iconostasis, which was gilded by Moscow masters in 1701. The icons were painted by Nikolai Solomonov and his assistants. The walls, portals, columns, and frames of the cathedral were decorated by craftsmen according to Yakov Bukhvostov's design. On August 15, 1702, Metropolitan Stefan Yavorsky consecrated the new Assumption Cathedral.

In 1800, the residents of Ryazan learned from the Most Reverend Simon Lagov that the Holy Synod had ordered the dismantling of the cathedral due to "dangerous dilapidation" and the construction of a new one. Due to its height and open location, the storm blew off the domes and roof, cracks appeared in the vaults and walls, and the upper windows were broken. In winter, snow was blown into the church, and in summer, birds built nests in the iconostasis. Archbishop Simon asked the citizens to discuss the issue of helping the cathedral. Ryazan merchants G. V. Ryumin and P. A. Malshin invited an architect from Moscow, who determined that the cathedral could be restored. The merchants donated funds and hired craftsmen. By 1804, the cathedral was restored and consecrated again on August 15. Donations amounted to 69,100 rubles.

The main shrine of Ryazan was considered to be the miraculous Theodotievskaya icon of the Mother of God, which appeared in 1487 in a field near the village of Theodotyevo. In its honor, celebrations were held annually on July 2. Another miraculous icon, the Murom icon, is older. It was blessed by Prince Svyatoslav for his son Prince Konstantin of Murom for his reign and the spread of Christianity. Saint Basil, Bishop of Ryazan, prayed before this icon in 1288. The cathedral also housed an ancient image of John the Baptist.

After 1917, church services in the temple ceased. The frescoes on the columns and walls were ruined by whitewashing, and the icons and property were requisitioned. For some time, a planetarium operated in the temple, and later museum exhibitions were held. In 1992, the cathedral was returned to the Ryazan Diocese and consecrated again on June 13. On that day, Archbishop Simon Novikov held an all-night vigil, and on June 14, on the Feast of the Holy Trinity, a Divine Liturgy was conducted. By the 900th anniversary of Ryazan in 1995, the restoration of the ancient iconostasis was completed.