[1][2] The city provided the four-acre waterfront site for the construction of the original building and The Junior League of St. Petersburg offered resources for The Great Hall.

"[3] Chartered by the State of Florida in 1961, the MFA opened its Beach Drive doors to the public in 1965; the first art museum in St. Petersburg.

The size of the museum was more than doubled in 2008, when the 33,000 square-foot Hazel Hough wing on the north side of the building was completed.

On June 23, 2022, a Bahamian artist, Gio Swaby, celebrated Black women at Museum of Fine Arts.

The museum's exhibitions have displayed Chihuly Across Florida: Masterworks in Glass (2004); Monet’s London, Artists’ Reflections on the Thames, 1859–1914 (2005), and Ancient Egypt: Art and Magic, Treasures from the Fondation Gandur Pour l’Art/Geneva (2011–2012), Moon Museum: Art and Outer Space (2018), Syd Solomon: Views From Above (2018-2019), Art of the Stage: Picasso to Hockney (2020), From Margins to Mainstays: Highlights from the Photography Collection (2021), Explore the Vaults: Cabinet Pictures and Works on Paper (2022), True Nature: Rodin and the Age of Impressionism (2023), and more.