Theatre Tallahassee was founded in 1949 as the Tallahassee Little Theatre and debuted with its first production, Boy Meets Girl, later that year. Incorporated as a nonprofit in 1952, the organization was established to promote community appreciation of the literary and dramatic arts.

Over the decades, Theatre Tallahassee grew steadily, gaining a permanent home in the late 1950s and expanding its facilities and programming to include a long-running five-play Mainstage season, summer productions, black box theatre, and special events. A major expansion in the early 1990s culminated in the dedication of its modern facility in 1994, featuring a 259-seat auditorium and enhanced performance spaces, marking nearly 45 years of continuous commitment to community theater in Tallahassee.