Holy Apostles College and Seminary was founded in 1956 on a 40-acre (160,000 m2) property in Cromwell, Connecticut, 13 miles (21 km) south of Hartford, by the Very Reverend Eusebe M. Menard, O.F.M., to provide a program of education and formation for men intending to enter the priesthood. Holy Apostles was then a college level, preparatory seminary, which Father Menard entrusted to the Missionaries of the Holy Apostles. After 16 years of operation, Holy Apostles, in accordance with the directives of Vatican Council II as well as, according to the college's website, its responsibilities to the larger Christian community, began admitting non-seminarians, women included.

The school is a regionally accredited college and seminary, recognized by New England Association of Schools and Colleges and the State of Connecticut; this includes its distance learning degrees. Members of its Board of Directors include the bishops of Connecticut with the Bishop of Norwich as Chancellor.

Programs offered include Associate of Arts and Bachelor of Arts degrees (added in 1972), a graduate program enabling students to earn Master of Divinity degrees (1978) with the college's creation of a Master of Arts program four years later. Holy Apostles' graduate program was expanded in 1998 with its move to offer a the Post Master’s Certificate in Theology as well. That same year, the school's Distance Learning Program was added to allow students to earn a Master of Arts degree in Theology or Philosophy via the Internet. Also offered is a Certificate Program designed to allow students to perform postgraduate study without enrolling in a Master of Arts program.