The church was first built in Moscow thanks to Lieutenant General M.A. Dukhonin and his wife, along with merchant Kaverin, in honor of Emperor Alexander III. In 1895, it was relocated to the city of Oryol.

The wooden church, consecrated in the name of the Resurrection of Christ, was established at Afanasyevsky Cemetery, which was founded in 1887 as the cemetery of the Vvedensky Convent. The name "Afanasyevsky" cemetery was derived from the eponymous settlement, where the Vvedensky Convent was established in the late 17th century. This name also became associated with the church. In 1897, the cemetery was enclosed with a stone fence, and a bell tower was built over the entrance, which was demolished in the 1930s. The church was wooden, standing on a stone foundation.

It was the only church in Oryol that always remained a church building and belonged to the community of believers. Services in the church were held with small interruptions until 1996. The wooden church completely burned down on the night of October 5 to 6, 1996. The modern stone building of the church was built later. In September 2001, Archbishop Paisiy of Oryol and Livensky consecrated the new stone church, erected on the same site according to the design of architect M.B. Skorobogatov.