A description of the church's foundation has been preserved: On August 16, 1821, after the early Divine Liturgy, the abbot Daniel arrived at the site of the foundation, made three prostrations to the east, and said: "May the blessing of the holy Jordanian desert and all those who are silent there be upon this place." After these words, the abbot took a spade and began to dig a trench for the church's foundation. On August 18, after the Divine Liturgy, a small procession without bells passed from the monastery to the skete. After a moleben with the blessing of water, the church was laid in honor of the Assembly of the Great and Glorious Prophet, Forerunner, and Baptist of Christ, John. A part of the relics of the saint was placed under the altar of the church, and the day ended in spiritual joy.

The church was wooden, built from timber cut on the site of the skete's clearing. Six months later, the construction was completed, and the church was equipped with the necessary utensils. The consecration was performed by the monastery's abbot, Daniel, on February 5, 1822, with a procession from the monastery.

By the blessing of St. Philaret, the church was arranged as a "house church for archbishop visits." In the western part of the church, a cell was arranged where the saint stayed during visits to the skete.

In 1863, the new skete head, the venerable elder Hilarion, began to implement a plan to raise the Forerunner's church and replace two lower rotting crowns. Many spiritual children of the deceased elder Macarius, who passed away in 1860, wished to honor his memory by establishing an altar in the church in honor of his Angel, the venerable Macarius the Great. However, this was impossible in the western part of the church due to the cramped conditions. In 1864, the church was reconstructed: the western part was dismantled and replaced with a more spacious annex. The entire building was raised by 0.9 m, with a new brick foundation and basements laid. The ceiling in the western part was raised to the level of the main church. The new annex became 2.8 m longer and wider than the previous one. An altar was arranged in honor of the venerable Macarius the Great, with its altar located in the southeastern part. A new altar and sacrificial table were installed in the central altar. The consecration of the main altar was performed by the abbot of the monastery, Venerable Isaac, on August 29, 1864, and the Macarius altar was consecrated by Bishop Gregory of Kaluga on September 7, 1864.

The revolution disrupted the prayer life of the skete. In February 1918, a detachment of Red Army soldiers came to the skete in search of gold and silver but found nothing. However, during the inspection, the holy vessels were desecrated. On January 19, 1918, St. Tikhon anathematized those who raised their hands against the church's sanctities. The day after the incident, a moleben was served, and the sanctities and church were consecrated. Soon, the monastery became an agricultural artel, and a museum was established in the skete. The Church of John the Forerunner was closed for many years.

In 1988, monastic life resumed in Optina Pustyn. On March 18, 1990, on the Sunday of the Cross, Metropolitan Vladimir of Rostov and Novocherkassk consecrated the Church of John the Forerunner. In 2002, the walls of the church were painted. Services in the church are held according to a special skete rule, with night services.