In 1778, with the establishment of the Oryol province, a new site was allocated for the cemetery outside the city. There was no church at this cemetery for almost half a century, and only in 1823 did the Oryol Spiritual Consistory permit the construction of a stone church funded by donations. In May 1828, the church in honor of the Life-Giving Trinity was consecrated, and services began in September of the same year. In 1849, the church porch was paved with stone, and wooden fences were installed around the building. Over time, the church was significantly expanded, and in 1864, its reconstruction began, culminating in the consecration in 1867.

Initially, the bell tower of the Trinity Church consisted of two pillars with a crossbeam. In 1838, they were replaced with new oak pillars with a wooden roof, which lasted until 1850. In 1851, fundraising began for the construction of a stone bell tower, completed in 1854.

After the revolution, the Trinity Church became part of the Renovationist movement. In 1929, the rectory was confiscated and occupied by residents, and in the winter of 1930, the bells were removed. The church continued to function for several more years but was closed in the mid-1930s. By the beginning of the Great Patriotic War, it was no longer operational. The last functioning church in Oryol, the Resurrection of Christ at the Afanasyevsky Cemetery, closed in 1941.

In 1944, the Trinity Church was handed over to the church community for free use. In 1979, the altar was painted, and in 1980, a separate entrance was arranged from the north side along with a small extension. In 1983, water supply was installed, and a well for draining water was created.

By 1990, the first floor of the rectory was converted into a church in honor of St. John Chrysostom, while the second floor housed a Sunday school and a library, which opened in 1991. In the mid-1990s, a chapel was built at the church.

From 2011 to 2013, restoration of the monumental painting on the dome was carried out, the plaster was reinforced, cement and gypsum inserts were removed, disinfection was conducted, cracks were sealed, and the painting was recreated.

In 2013, during the restoration, historians and local historians discovered that some graves had been looted in the 1930s-1950s. Employees of the Institute of Archaeology of the Russian Academy of Sciences surveyed the memorial and collected the remains. In 2014, a recreated crypt of General Alexei Petrovich Yermolov and his family was opened in the church. The memorial was restored and returned to its original appearance.

In the military cemetery next to the church, soldiers who fell in battles for the liberation of Oryol in 1943 are buried.