Babbitt began his aviation career as a pilot, flying 25 years for Eastern Airlines. A skilled negotiator, he served as President and CEO for US ALPA, the world's largest professional organization of airline pilots. While at ALPA, he championed the "One Level of Safety" initiative implemented in 1995 to improve safety standards across the industry. He also promoted the international expansion of ALPA through a merger with the Canadian Air Line Pilots Association in 1997. 

During the Clinton Administration, President Bill Clinton appointed Babbitt to the FAA Management Advisory Council. While in that capacity Babbitt sat on an independent review panel advising the government on aviation safety policy.  

President Barack Obama formally nominated Babbitt to become the sixteenth FAA Administrator on March 27, 2009, after more than eight years on the agency's Management Advisory Council providing guidance to other Administrators on a range of topics ranging from air traffic modernization to regulatory policy and safety oversight within the airline industry and the FAA. 

Babbitt's nomination was confirmed by the US Senate on May 21, 2009; he was sworn in on June 1. Babbitt succeeded Robert Sturgell and Lynne Osmus, who had both served as Acting FAA Administrator since Marion Blakey's term expired in 2007. Babbitt's FAA term was five years. During his confirmation hearing Babbitt stated "My number one priority is to focus on safety. This is a business where one mistake is one too many."