The village of Krasnoye is first mentioned in historical documents in 1569, when its owner was the chamberlain I.D. Vorontsov, a descendant of the murza Cheta, who, according to legend, founded the Ipatiev Monastery in Kostroma. After the inclusion of the Kostroma district into the oprichnina lands, all owners, including Vorontsov, were evicted from Krasnoye. The village became a palace property and was managed by the Order of the Grand Palace, later passing to the Godunov family.

In 1592, Boris Godunov built a stone tent church of the Epiphany here, as indicated in the clerical records. The chapels and the two-tiered gallery of the church were built simultaneously with the temple, the bell tower appeared in the 17th century, and the western narthex in the 18th century. The church was repeatedly rebuilt, and by the end of the 19th century, only the tent remained of its original appearance.

The church was closed in 1932, after which it was used as a library, warehouse, club, and grain storage, which severely damaged its interior decoration. In the 1950s-1960s, I.Sh. Shevelev carried out repair and restoration work, restoring the appearance of the church to that of the late 17th century. In the 1990s, another restoration took place: the church was painted in the spirit of Orthodox painting of the 16th-17th centuries, the lower tier of the gallery was bricked up, and the upper tier was glazed.

In 1990, the church was returned to the Kostroma and Galich diocese, but the restoration that began in 1950 continued. The complete restoration was completed on August 6, 2009, when a grand consecration took place. The consecration and Divine Liturgy were conducted by Archbishop Alexander of Kostroma and Galich, with the clergy of Kostroma and the Krasnoselsky deanery serving alongside him. The current rector of the church is Archpriest Grigory Kovalsky, the dean of the Krasnoselsky deanery.

In the late 19th century, next to the Church of the Epiphany, a Church of the Holy Apostles Peter and Paul was built with public funds. This architectural ensemble was surrounded by a fence, in front of which stood a monument to Emperor Alexander II. Inside the fence was a cemetery. During the period of persecution against the church, the monument to Alexander II was destroyed, the church was blown up, and the cemetery was desecrated.