The MFA was founded by art collector and philanthropist Margaret Acheson Stuart. As its first president, Mrs. Stuart contributed significantly to the construction of the building and provided endowment funds through her estate to support annual operations and to maintain the beauty of the grounds. She also provided monies to acquire art and donated works from her collection. The Margaret Acheson Stuart Society, the Museum's independent support organization, is named in her honor. 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. The building was designed by John Volk and Associates of Palm Beach, with a curving colonnade on Beach Drive. Volk stated that "a museum should give a feeling of permanence and that is what I have tried to do with this building." 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 Marly Room, an auditorium seating 220, and a sculpture garden, both made possible by Mrs. Stuart, were added to the building in 1974.
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