The first mention of the church dates back to 1628. In the early 17th century, there was a complex of two wooden churches on this site: a "winter" church dedicated to the holy martyrs Flora and Lavra, which gave its name to Lavrovskaya Street, and a "summer" church dedicated to John Chrysostom. The Kostroma census book mentions: "On Zlatoosten Street in Kuznetsy, there is a wooden church of the holy martyrs Flora and Lavra, and the church site of John Chrysostom." By the time the book was compiled, the last church had likely burned down, leaving only the "church site."

In the 17th century, the wooden church of John Chrysostom was restored, and by the mid-18th century, a five-domed stone church was built in its place, consecrated in 1751.

The stone church of John Chrysostom and the wooden church of Flora and Lavra stood side by side for about 40 years. The stone church was "cold," and winter services were held in the wooden church of Flora and Lavra. By the end of the 18th century, it had fallen into disrepair, and two "warm" chapels and a bell tower were added to the west of the John Chrysostom church. These chapels, topped with small domes, increased the number of domes of the church to seven and were consecrated in 1791.

In the spring of 1922, as part of the all-Russian expropriation of church valuables, over 117 kg of silver items were confiscated from the church of John Chrysostom: icon covers, sacred vessels, and lamps.

That same year, the historic cathedral churches in the former Kostroma Kremlin fell into the hands of the Renovationists, and the new cathedral became the church of the holy prophet Elijah on Rusinskaya, now Soviet Street. When it was closed in November 1929, the cathedral became the church of St. John Chrysostom.

In 1959, Bishop Sergey Kostin of Kostroma was buried in the churchyard.

In 1964, the Kostroma Cathedral was moved to the Church of the Resurrection of Christ on Debra, and the church of John Chrysostom became a dependent church. During N.S. Khrushchev's rule, authorities planned to close and demolish it. It only regained the status of an independent parish church in 1966.