It was founded in 1886 as St. Ignatius College and renamed in 1923 after John Carroll, the first Catholic bishop in the United States and founder of Georgetown University.

[7] In September 1968, the university made the transition from full-time male enrollment to a fully coeducational institution, admitting women to the College of Arts and Sciences for the first time.

In 2011, the university completed the removal of the Bohannon Science building and celebrated the Hamlin Quad enhancement project.

The university announced in December 2017 that its board of directors had named the school's first non-Jesuit president, Michael D. Johnson.

[8] More than twenty major buildings, predominantly Collegiate Gothic in architecture, and sixty landscaped acres make up the John Carroll campus.

Saint Ignatius Hall, located in the center of campus and surmounted by the university's landmark Grasselli Tower, bears clear resemblance to the English royal palace Hampton Court.

[9] John Carroll University's College of Arts and Sciences offers more than 80 distinct programs for undergraduate and graduate students.

[11] These programs include the Belfast Institute in Peace Building and Conflict Transformation,[12] the Boler School of Business Semester in London,[13] Italian Studies at Vatican City, the London Liberal Arts Semester, the Jesuit Beijing Center, as well as Casa de la Solidaridad in El Salvador.

Fraternities and sororities are approved by the John Carroll University Office of Student Activities and governed by the rules of the Interfraternity and Panhellenic Councils.

The university plays football, lacrosse and soccer in Don Shula Stadium, named after the winningest coach in NFL history, who had studied at John Carroll between 1947 and 1951.

On November 12, 2016, John Carroll defeated the University of Mount Union 31–28, snapping the program's college football record of 112 straight regular season wins.