
Faulkner University was founded as the Montgomery Bible College in September 1942 by religious educators and preachers Rex Turner, Calvin Leonard Johnson, and Joe Greer. The three also established Churches of Christ congregations in Alabama. Turner and Johnson would serve as school co-presidents in its early years and as presidents of its several derivative schools. The college, located on Ann Street near downtown Montgomery, initially offered four years of high school curricula and one year of college but soon expanded to provide elementary and secondary schooling and junior college classes. In 1953, the school was renamed the Alabama Christian College (ACC). It moved to its present location on Atlanta Highway in 1964.

The ACC's elementary and secondary departments had been separated out from the college in a new facility in 1965 and named the Alabama Christian High School and Elementary School. In 1985, a new campus for upper grades was opened next to Faulkner University. Elementary grades followed in the early 1990s. It is now the present-day Alabama Christian Academy, a K-12 institution. The ACC's upper-level religious studies program had been discontinued in the mid-1960s to facilitate ACC's accreditation as a junior college, and the faculty and curriculum were housed in the new Alabama Christian School of Religion. It later became Southern Christian University, then Regions University, and is now present-day Amridge University located next to Auburn University Montgomery.
Faulkner University has more than 3,500 enrolled students, including some 2,000 undergraduates, and offers more than 60 on-campus majors and 23 online majors. Faulkner University is accredited to award degrees at the associate, baccalaureate, master's, and doctoral levels, including the online degrees. There are five colleges; the College of Arts and Sciences, the V.P. Black College of Biblical Studies, named for Vanderbilt Pierpont Black, a former school vice president and financial supporter, the College of Education, the College of Health Sciences, and the Harris College of Business and Executive Education, in addition to the law school. The Montgomery campus offers associate degrees in computer and informational science and legal studies and associates of arts or sciences in the liberal arts. It also offers numerous bachelor degree programs and some masters and doctoral degrees. The Birmingham, Huntsville, and Mobile campuses offer associate degrees in computer and information science and legal studies and associates of arts or science in the liberal arts, a variety of bachelor degree programs in the behavioral sciences, business, criminal justice, and more.

The university has two choral programs, the Faulkner University Chorus and the Faulkner Singers, and a marching band. The Chorus performs locally and regionally and also takes part in an annual spring tour in which the group travels across the United States. The Faulkner Singers is a smaller group, with only 16 singers chosen from the Faulkner University Chorus. In fall 2010, the Faulkner University Marching Band was established and has continued to increase in members every season.
Faulkner University supports teams in men's baseball, basketball, soccer, football, and golf, and women's basketball, golf, soccer, softball, and volleyball. The baseball team won the national championship in the National Christian College Athletic Association in 2001. Faulkner is part of the National Association of Intercollegiate Athletics, the Southern States Athletic Conference, and the Mid-South Conference. The mascot is the Eagles.