Headed by an Administrator who is appointed by the President of the United States, the FTA functions through Washington, D.C. headquarters office and ten regional offices which assist transit agencies in all states, the District of Columbia, and the territories.

The FTA oversees grants to state and local transit providers, primarily through its ten regional offices.

President Kennedy stated, "To conserve and enhance values in existing urban areas is essential.

But at least as important are steps to promote economic efficiency and livability in areas of future development.

President Lyndon B. Johnson signed the Urban Mass Transportation Act of 1964 into law, which passed the House by a vote of 212-129 and cleared the Senate 52–41, creating the Urban Mass Transportation Administration.