The theater opened in 1915 in a Court Street storefront that had previously housed the Bethel grocery store, under the name Majestic Theatre. A 'four reeler' cost five cents - dramatically less than the Athens opera house, which the Majestic was designed to undercut. The booking strategy was first-run films at a price that any student or townsperson could afford, and it worked. The opening year drew customers to Etta of the Footlights and A Good Little Devil and the other photoplays of 1915 cinema. Ohio's censor board, however, was active. Birth of a Nation was banned in the state for two years; even after the censors permitted it, Ohio viewers had to travel to Columbus or Cincinnati to see it. Theda Bara's Sin was permitted only after the theater repackaged it as 'a depiction of what would happen if one commits a sin' - a study of human behavior rather than entertainment.

The Majestic was renamed the Athena Theatre around 1935 when new owners took over, and by the early 1940s it was being operated by the Schine Circuit - one of dozens of small-town theaters the Schine family operated across upstate New York, Ohio, and Kentucky. The name Athena, taken from Athens, Ohio, eventually replaced the Schine prefix, and the theater operated for the rest of the century as a private movie house. By 2001 the business was for sale and finding no buyer. The building had been adapted into a multi-screen art-house format somewhere along the way, but as a stand-alone enterprise it could no longer cover its costs. Ohio University took over the property, restored the building, and reopened it in February 2002 under an outside management contract.

Student involvement in the theater has often taken the form of friendly antagonism. In May 1968, the Athena announced that adult tickets would rise from $1.50 to $2.00. Two undergraduates began picketing the box office on a Friday night. By Monday, the picket line had grown to twenty. The theater's management sat down with the students and agreed to a compromise: a $1 matinee price for shows before 5 p.m., with $2 evening tickets. The deal was supposed to be a trial. The trial became permanent. Forty years later, the same matinee-and-evening split is still how American movie theaters price their tickets - a system that, at least in Athens, was bargained into being by two undergraduates with hand-lettered signs.

Scandals over content recurred. In 1972, the Athena pulled Sexual Freedom in Denmark after complaints from townspeople, replacing it with No Deposit, No Return; Mayor Donald Barrett sent the police captain to view the original to assess whether the complaints were warranted. In February 1977, a manager named Ben Geary screened a film called Fantasy Girls, and the Athens police chief, Ted Jones, came to ask him to stop showing X-rated films. Geary pulled Fantasy Girls but refused to drop A Clockwork Orange - which was widely considered respectable cinema despite its content. A few days later, Jones reversed course publicly, saying he was 'not comfortable with police officers making decisions' about what constituted obscenity. Geary won the argument. The Athena kept showing serious films that other theaters wouldn't.

Since September 2008, the Athena has been operated by Ohio University's College of Fine Arts. The director is Alexandra Kamody, herself an Ohio University alum and former Athena student worker. The theater employs more than forty students through Federal Work Study, who run projection, manage concessions, sell tickets, and program the calendar. The programming leans art house and international, with regular screenings during the Athens International Film and Video Festival in spring. It is a working educational venue: students learn the business of cinema operations while continuing to bring eclectic films to a small Appalachian college town.

From the air, the Athena reads as one storefront among many on Court Street - the main commercial spine of uptown Athens, three blocks long, lined with restaurants and shops. The theater's vertical marquee, illuminated at night, identifies the building from street level but disappears at altitude. The College Green of Ohio University, with its red-brick academic buildings arranged around grass and elm trees, sits a single block south. The Hocking River bends around the campus to the east. The whole town is small enough that the theater, the campus, the football stadium, and the surrounding hills can be taken in from one low pass.