Alabama State University was founded in 1867 as the Lincoln Normal School of Marion in Marion. In December 1873, the State Board accepted the transfer of title to the school after a legislative act was passed authorizing the state to fund a Normal School, and George N. Card was named president. Thus, in 1874, this predecessor of Alabama State University became America's first state-supported educational institution for blacks. This began ASU's history as a "teachers' college."

In 1878, the second president, William Paterson, was appointed. He is honored as a founder of Alabama State University and was the president for 37 of the school's first 48 years. Paterson was instrumental in the move from Marion to Montgomery in 1887. 

In 1887, the university opened in its new location in Montgomery, but an Alabama State Supreme Court ruling forced the school to change its name; it was renamed the Normal School for Colored Students. The campus was chosen in 1889 although preparing the buildings at the site took a while longer.[4] 

In the decades that followed, Lincoln Normal School became a junior college, and in 1928 became a full four-year institution. In 1929 it became State Teachers College, Alabama State College for Negroes in 1948, and Alabama State College in 1954. In 1969, the State Board of Education, then the governing body of the university, approved a name change; the institution became Alabama State University.

The 1995 Knight vs. Alabama remedial decree transformed ASU into a comprehensive regional institution paving the way for two new undergraduate programs, four new graduate programs, diversity scholarship funding and endowment, funding to build a state-of-the art health sciences facility, and a facility renewal allocation to refurbish three existing buildings.

WVAS-FM was launched on June 15, 1984, beaming 25,000 watts of power from the fifth floor of the Levi Watkins Learning Center for two years before moving to its current location at Thomas Kilby Hall. Today, WVAS has grown to 80,000 watts and has a listenership that spans 18 counties, reaching a total population of more than 651,000. In recent years, the station has also begun streaming its broadcast via the Web, connecting a global audience to the university.

The early 1990s witnessed the beginning of WAPR-FM (Alabama Public Radio), which Alabama State University and Troy University, both of which already held station licenses of their own, cooperated with the University of Alabama in building and operating. WAPR-FM 88.3—Selma's signal reaches the region known colloquially as the Black Belt, about 13 counties in the west central and central parts of Alabama, including the city of Montgomery.