Theatre Downtown was founded in 2006 by Billy Ray Brewton and Cindy deSa, and is now operated by a Board of Directors as a 501(c)3 non-profit entity. Originally located inside the former Playhouse location on Third Avenue North, Theatre Downtown moved from there to a temporary basement location at Birmingham AIDS Outreach before moving to the Fifth Avenue Antiques location in 2009. After losing its home in 2019, Theatre Downtown went on a temporary hiatus during the COVID-19 pandemic and re-emerged in 2024 with a brand new home on Fourth Avenue South.