From 1641 to 1646, after the city of Oryol was burned by the Poles and Lithuanians, restoration began, during which a church was built in the name of the Epiphany of the Lord at the settlement in the Great Ostrog. Over time, a male Epiphany Cathedral arose beside it.

After a fire in 1680, the church was moved a verst downstream of the Oka River and became a parish church. The stone building of the Epiphany Cathedral in Oryol was erected in the early 18th century, as confirmed by its architectural forms. The original appearance of the building, preserved in drawings and photographs, was slender and richly decorated, belonging to the style of "Naryshkin Baroque," popular among the boyars close to the royal court.

In 1837, the cathedral underwent a major reconstruction, resulting in massive apses and new classicist porticos, although the main parts of the building and the bell tower remained unchanged. In 1900, it was recognized that the bell tower was at risk of collapse, and it was dismantled. In 1908, construction began on a new bell tower with two towers in the pseudo-Russian style, which dominated Russian architecture in the late 19th and early 20th centuries. The tiers of the bell tower were decorated with kokoshniks and small domes.

Since 1900, the church was led by Archpriest Ilya Vasilyevich Livansky, who became the chairman of the Oryol Church Historical and Archaeological Society in 1906.

In 1939, the bell tower of the Epiphany Cathedral was again destroyed. During the war, a small deaf octagon and a dome with a cross were shot down. In 1948, the cathedral was under the care of the faithful, and preparations for repair and restoration work began. In 1952, a new dome was installed, and in 1956, a Moscow artist partially painted the refectory of the church. In 1957, the old painting of the main volume was restored.

In 1964, the cathedral was converted into a city puppet theater, for which the dome of the church was dismantled, the crosses were removed, and the internal dome space was covered with a flat ceiling.

In 1994, the cathedral was handed over to the community of believers, and on April 6, 1996, it was consecrated by Archbishop Paisiy of Oryol and Livny.