The Seminary was founded in 1976, and offered courses to 35 students in its first year of operation. Being before the age of World Wide Web, all instruction in those early years was done either by correspondence through the mail, or face to face.

Initially, the Seminary was the official training program of the Alexandrian Orthodox Exarchate of the West and was called the Pan-American Institute of Apostolic Christianity. When the Exarchate was received into the American Church in 1987, by Archbishop Denis, the Seminary became the school of the Archidiocese of the Resurrection, in Denver, Colorado. That year the name was also changed to honor Saint Innocent, the first Orthodox Bishop of North America.

When the Church was split with the schism of her bishops in the mid-1990's, there was initially some disagreement as to the ownership of the name of the seminary. For a brief time, the Seminary was known as Saint Gregory the Theologion, to reduce confusion with another training program being offered by the schismatic faction of bishops. With the end of the schism, the Church, now known as the Russian Orthodox Church in America, reclaimed the name of the Seminary for her official teaching institution.

We are the only Orthodox Theological Seminary that offers our training by distance learning and in the five languages used in the Western Hemisphere.