[2] In 1864, wealthy Boston merchant James Stanworth acquired a farm on a hill in Brighton known as the Hildreth estate.

Archbishop John Joseph Williams purchased the Hildreth estate and construction of the Boston Ecclesiastical Seminary[3] began in 1881 and was completed in 1884.

In 1911, the Sulpicians withdrew from the seminary at the request of Archbishop William Henry O'Connell,[5] who preferred a diocesan faculty more familiar with local conditions.

St. John's College Seminary, the division for students with a high school diploma but without an undergraduate degree, closed in 2002.

[9] In the wake of the Catholic Archdiocese of Boston sex abuse scandal enrollment declined from a peak of 86 students in the academic year 2001–02 to 34 for 2005–06.

In 2001, Boston College leased St. Clement's Hall, formerly the site of the Seminary's undergraduate division, and it bought the property in June 2004.

[15] In August 2018, the rector of Saint John's was placed on administrative leave after two former seminarians claimed on social media that sexual misconduct occurred at the school.

[17] On November 22, 2019, the Archdiocese of Boston and former U.S. Attorney Donald Stern concluded that there was some accuracy to the 2018 allegations, such as the expulsion of two students in 2014 for inappropriate sexual conduct, an incident from 2015 where six students received anonymous sexual text messages, and excessive drinking at a 2015 bachelor party which was held on campus.

As a major seminary, an institution providing formation for the Catholic priesthood, Saint John's offers a four-year program leading to the Master of Divinity degree.

[25] In addition, "Saint John's Seminary offers a two-year program of initial formation for those candidates who are college graduates and have no prior experience of formal preparation for the sacrament of Holy Orders.