The first purpose-built Orthodox Christian church to open in Japan was the wooden Russian Consulate chapel of the Resurrection of Christ, in Hakodate, Hokkaidō, consecrated in October 1860.

[3][4] In July 1861, the young Russian Hieromonk Nikolay Kassatkin (subsequently canonized and known as Nicholas of Japan), arrived in Hakodate to serve at the consulate as a priest.

Kassatkin travelled across Russia to collect funds for the construction of the Orthodox Cathedral in Tokyo, which was inaugurated in Kanda district in 1891 and went on to be known after him as Nikorai-do.

Following the surrender of Japan (August 1945), the Allied occupation regime had a benevolent attitude toward Christian groups, given their predominantly American connections.

In 1946, the precursor to the Orthodox Church in America (OCA), the Metropolia (a de facto independent jurisdiction at the time), on the initiative of U.S. Army Colonel Boris Pash, took steps to prevent the Moscow Patriarchate from re-establishing its control over the Japanese Church - despite the vigorous efforts Moscow undertook to this end.

[12] The following year the Japanese Church largely switched to come under the Metropolia′s jurisdiction, and would be governed by bishops sent from the U.S. by the Metropolia until March 1972.

As the Metroplia in the late 1960s gradually restored relations with the Moscow Patriarchate (whose external activity was fully controlled and guided by the Soviet government and specifically by the KGB[13]) with a view to obtaining autocephaly (i. e. legitimate administrative independence), the Japanese Church transferred to Russian Orthodox Church jurisdiction.

The abbot of the monastic community, Hieromonk Gerasimus (Shevtsov) of the Troitse-Sergiyeva Lavra, dispatched by the Holy Synod of the Moscow Patriarchate,[17] arrived in Japan at the end of 2005.

[20] As of the end of 2014, according to the data provided by the Ministry of Culture of Japan, the church had a total of 67 parishes (communities), 37 clergymen, and 9,619 followers (registered members).

The seminary accepts only male faithfuls and gives a three-year theological education to those who expect to become ordained presbyters and missionaries.

As of the end of 2021, according to the data provided by the Ministry of Culture of Japan, the church had a total of 64 parishes (communities), 25 clergymen, and 9,249 followers (registered members).