There are several legends about the founding of the monastery, which differ in details. According to one of them, there was a wooden chapel in honor of Saint Great Martyr Dimitri of Thessalonica and a hermit's cell at the site of the monastery. The troops of Dmitry Donskoy, heading to battle against Khan Mamai, stopped at this chapel. Alexander Peresvet, preparing for battle, prayed in the cell and left his apple staff there. According to another version, the chapel was built by Dmitry Donskoy himself in honor of his angel, the Great Martyr Dimitri of Thessalonica, stopping at Dmitrievaya Hill by the Verda River to celebrate victory at Kulikovo Field.

Some studies suggest that these legends may refer to the Trinity Monastery, which later became known as the Skopin Holy Spirit Monastery, located closer to the city of Skopin. In the 17th and 18th centuries, the Trinity Monastery was closed and reopened several times. It is possible that during one of these closures, Peresvet's staff was transferred to the Holy Dimitrievsky Monastery, along with the legends.

Despite the differences in the legends, the staff of Alexander Peresvet, known as "Peresvet's club," is a real relic that was kept in the monastery for 600 years and is now housed in the Ryazan Regional Museum.

The first written mention of the monastery dates back to 1676, which refers to the wooden churches of Dimitri of Thessalonica, built in 1660, of Sergius of Radonezh, erected in 1667, and the monastic cells.

In the 1760s-70s, the monastery was rebuilt with merchant donations. Stone churches replaced the wooden ones: the cold church of Dimitri of Thessalonica and the warm church of Sergius of Radonezh, as well as utility buildings.

In the early 19th century, the dilapidated church of Dimitri of Thessalonica was reconstructed and repainted. Services resumed there in 1829, but finishing and painting continued until 1854. In 1863, the brick refectory was converted into a church in honor of the icon of the Mother of God "Joy of All Who Sorrow." At this time, a stone fence and a three-tiered bell tower were built around the monastery.

In 1918, the monastery was closed, its buildings nationalized, and transferred to a collective farm. The monastery housed warehouses, pigsties, and a school. Monastic relics and icons were partially transferred to museums and partially destroyed. Subsequently, the collective farm was reorganized, and the buildings were dismantled for construction materials.

Restoration of the monastery was deemed impossible, and only ruins remained at its site.

On October 21, 1995, Bishop Simon of Ryazan and Kasimov consecrated the church of Dimitri of Thessalonica.

On January 4, 1996, by decree of the Holy Patriarch and the Holy Synod, the parish of Dimitri of Thessalonica was transformed into the Holy Dimitrievsky Men's Monastery.

On June 1, 1996, the first tonsure took place.

By early 2010, the churches, bell tower, fence, and utility buildings of the monastery were fully restored. An icon-painting workshop is operational. There are 5 members of the brotherhood living in the monastery.

The monastery houses relics such as a part of the relics of St. Sergius of Radonezh, parts of the relics of the Optina Elders, and a part of the relics of St. Theophan the Recluse.