Designed by Yann Weymouth, the museum is located on the downtown St. Petersburg waterfront by 5th Avenue Southeast, Bay Shore Drive, and Dan Wheldon Way.

[7] Shortly before marrying in 1942, Reynolds and Eleanor Morse attended a Dalí retrospective at the Cleveland Museum of Art.

A Wall Street Journal article titled "U.S. Art World Dillydallies Over Dalí" caught the attention of the St. Petersburg, FL community, who rallied to bring the collection to the area.

[10] A marine warehouse in downtown St. Petersburg, Florida was rehabilitated and the museum opened on March 7, 1982,[9] where it remained until 2010.

Located on the downtown waterfront next to the Mahaffey Theater, on the former site of the Bayfront Center (an arena which had been demolished in 2004), the new, larger, and more storm-secure museum was opened on January 11, 2011.

[13] The museum's collection includes 96 oil paintings, over 100 watercolors and drawings, 1,300 graphics, photographs, sculptures, and objets d'art, plus an extensive archival library.

The museum is home to more masterpieces of Dalí than any other museum in the world, including the large-scale paintings The Hallucinogenic Toreador, The Discovery of America by Christopher Columbus, The Ecumenical Council, Geopoliticus Child Watching the Birth of the New Man and The Disintegration of the Persistence of Memory.

The exhibit included 79 paintings, drawings, and collages, and was organized in collaboration with the Musée national Picasso-Paris.

Participants can walk around, through the desert, up the towers, and into hidden rooms within Dali's Archeological Reminiscences of Millet's "Angelus.