The history of the Orthodox Priestly Seminary began in 1948 under the name "Spiritual Seminary" with its headquarters in Karlovy Vary, and the following year it was moved to Prague.

In 1950, the Orthodox Faculty of Theology was established with its headquarters in Prešov, and at the same time, on the basis of government regulation no. 112 of June 14, 1950 pursuant to Act No. 66/1950 Coll. of the Czechoslovak Republic on universities.

In 1990, the faculty and the priestly seminary became part of the PJ Šafárik University in Košice. From January 1, 1997, the faculty and the priestly seminary were based on Act NR SR No. 361/1996 Coll. about universities incorporated under the University of Prešov in Prešov.

Since 1950, the Orthodox Faculty of Theology and Theological Seminary have been housed in a common building on Sládkovičová Street in Prešov. In 1989, due to government regulation and law, the faculty had to hand over the property to the original owner - the Greek Catholic Church. For that reason, the state assigned it premises, which the Orthodox Church had to reconstruct. The Orthodox Faculty of Theology was moved to Masaryková Street No. 15 and the Orthodox Priestly Seminary to Plzenská Street No. 7 in Prešov. The Priestly Seminary became an independent subject of the University of Prešov, although it remained part of the Orthodox Faculty of Theology.

As of September 1, 2003, the priestly seminary remains a part of the PBF PU in the educational process, but economically it is created as an independent entity of the University of Prešov in Prešov.

In the years 1991 - 2011, he was the director (rector) of the Orthodox Priestly Seminary. Mgr. Emil Jarkovsky. In the years 2011 - 2021, the rector was prot. Prof. Ph.Dr. Milan Gerka, CSc.

At the moment, the head of the Orthodox priestly seminary is protodeacon doc. Ph.Dr. Ján Husár, PhD., vice-rector.