Historian A. P. Nikulov believes that the cathedral church was laid in 1593, when the construction of the fortress city of Oskol began. In the 16th century, the Church of the Transfiguration of the Lord was wooden and located in the Small Ostrog, which later became the Lower Square. Its location remained unchanged for centuries, on the territory from the modern cinema "Oktyabr" to the chalk cliff above the Oskol River.

It is known that in 1596, chapels were added to the cathedral, but in 1616 the church burned down. A new fire occurred on June 14, 1628, from the newly built church in honor of the Nativity of the Blessed Virgin Mary. In 1629, the church was restored with a chapel in the name of Archangel Michael. From 1633 to 1635, it remained empty, as sources state, "the priest of Kurdyum was killed by Tatars, and there was no deacon."

Research by A. P. Nikulov shows that a new church was likely built in the first half of the 17th century. In 1715, it burned down and was restored the following year at the same location, opposite the western gates of the fortress. The construction of the brick church likely began simultaneously with the Assumption and Trinity churches and was completed by 1767. The main altar was possibly consecrated later, as another wooden church in the name of Guriy, Samson, and Aviva was in operation. The stone temple was located almost in the center of the fortress and remained unchanged until 1840.

Thanks to the efforts of merchant Alexei Ivanovich Ivanov, construction was completed by 1840. On August 15 of the same year, the temple was consecrated by Bishop Juvenaly (Polovtsev) of Kursk and Belgorod with the main altar in the name of the Epiphany of the Lord. The right altar was consecrated in honor of the icon of the Blessed Virgin Mary "The Sign," and the left, in the name of the Nativity of the Blessed Virgin Mary. The church built in 1840 featured beautiful architecture, with walls finished to resemble marble and gilded iconostases. Its length was about 43 meters, width over 34 meters, and height 37 meters.

A garden was arranged around the church through the efforts of church elder Mikhail Alexandrovich Ivanov on land donated by merchant Stefan Matveevich Kobozev.

In 1888, priest A. I. Plozhintsev of the Cathedral organized religious and moral readings, and later, the society for helping the poor opened "public popular readings" of books. In 1892, the society opened a Sunday school for illiterate adults, which was attended by more than a hundred people. A four-class church-parish school operated at the cathedral, whose graduates could continue their education at the Higher Primary School and the Real School.

In 1913, a sobriety society in the name of Saint Martyr Boniface was established at the Epiphany Cathedral.

In 1923, according to the Decree "On the Separation of Church from State," the cathedral building and all its property were transferred for free rental use to the religious community. In December 1929, the Starooskolskaya Diocese was formed, with the first bishop being Vladyka Onufriy (Hagaluk).

By the early 1930s, the authorities prohibited ringing the bells and began confiscating them. Over the first three decades of Soviet power, the Lower (Trading) Square changed beyond recognition. The main street of Stary Oskol, Kursk, was renamed International in 1918 and received the name Lenin in 1960. The cathedral disappeared from the square, and a park named after A. M. Gorky grew in its place. In this park stood a monument to V. I. Lenin, pointing north with his hand. Bricks from the destroyed churches were used to strengthen the pavement.