The first church at the cemetery of the village of Kovrovo was wooden and dedicated to the Protection of the Holy Virgin. In the 17th century, there was an altar in honor of St. John of Rila at this church, but by the end of the century, the church disappeared. A new church at the city cemetery of Kovrov was built in the 1780s and consecrated in honor of St. John the Warrior, the great martyr. This church was also wooden, did not have its own clergy, and was attached to the Christ-Birth Church of the city. Over time, it became dilapidated, and by the early 19th century, there was a need for a new church. In October 1810, titular adviser Pyotr Borisovich Oshanov and Kovrov merchant Ivan Fyodorovich Aparin appealed to the Vladimir Spiritual Consistory for permission to build a stone church. Oshanov donated 1000 rubles, and Aparin 500. The diocesan authorities instructed priest Alexander Mikhailovich Shirokogorov to inspect the old church and confirm the need for construction. In his report, Shirokogorov noted that the church was dilapidated and spoiled the appearance of the city. The consistory appealed to Bishop Xenophon of Vladimir and Suzdal for permission to build. In February 1811, the bishop granted permission to build a stone church with an altar, allowing the old wooden one to remain until the new one was completed. The church construction decree was signed on March 1.

The project for the new stone church was developed by Vladimir provincial architect Alexander Nikitich Vershinsky. In 1812, he was replaced by Yevgraf Yakovlevich Petrov, who changed the project after construction began in the spring of 1811.

In 1994, the church was returned to the Church. After restoration, it was reopened to parishioners. During the restoration work, a monument was found from the grave of the wealthy manufacturer Ivan Andreyevich Treumov. This gravestone is now installed at the northeast corner of the altar of the former cemetery church. In 1946, the famous weapons designer Vasily Alexeyevich Degtyaryov was buried in Pushkin Park. This is perhaps the only landmark of the former cemetery. Pushkin Park did not become a popular recreation area, and the residents of Kovrov often pass by the walls of the St. John the Warrior Church, unaware that they walk on the land of their ancestors.

In 2006, a Orthodox cross was erected at the site of the entrance chapel over the graves of the princes of Kovrov, a symbolic monument to many generations of Kovrov residents who found peace at the cemetery by the church of St. John the Warrior.