With origins dating back to 1743, it is now one of the City of Pensacola's Enterprise Operations, having been incorporated in 1943 as the Municipal Port Authority.

The group pressed State Representative Dave Thomas to introduce a bill in the Florida legislature creating the Municipal Port Authority in the spring term of 1943.

Its members were initially appointed by state senator and included J. D. Johnson, Henry Hilton-Green, Calvin L. Todd, William S. Rosasco, W. V. Fauria, Morris Levy, J. H. McCormack, J. W. Smith, Jr., Charles W. Smith, J. H. Allen and R. H. Turner, Jr. (Later members would be appointed by the Pensacola City Council, which also approved annual funding to the Port Authority, as it had no taxing authority of its own.)

In November 2018, the Port of Pensacola became the winter base for The New York Yacht Club American Magic, the United States Challenger in the 36th America’s Cup.

The New York Yacht Club American Magic, the United States Challenger in the 37th America's Cup, announced in June 2022 that it had returned to the Port of Pensacola to train.