The organization that would eventually become APTA first organized as the American Street Railway Association on December 12, 1882, in Boston, Massachusetts. The initial meetings focused on the price of oats for the horses that pulled transit vehicles, but that focus evolved as more transit companies built electric systems.

In 1905, the group met in New York and reorganized as the American Street and Interurban Railway Transportation and Traffic Association. To encompass even more modes of electric transit, the group changed its name to the American Electric Railway Transportation and Traffic Association in 1910.

By 1932, many of the transit systems relied on motor coaches and trolleys in addition to electric streetcars, so the organization became known as the American Transit Association (ATA).

In 1966, ATA relocated from New York City to Washington, DC because of increasing reliance on federal funding, especially with the passage of the Urban Mass Transportation Act in 1964 and the creation of the Urban Mass Transportation Administration (now the Federal Transit Administration).

In the 1970s, the organization developed a closer working relationship with the federal government as more and more transit systems became publicly financed. The American Public Transit Association (APTA) was created in 1974 when the American Transit Association and the Institute for Rapid Transit (IRT) merged. The IRT dated back to 1929 and formally organized on June 7, 1961. In 1976, the Transit Development Corporation also merged with APTA.

In January 2000 the name of the organization was changed to the American Public Transportation Association. Despite the various name changes, the mission of the organization has remained generally the same.

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