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All passenger and freight rail travel in the United States is subject to regulations enforced by the FRA. Most notably, the FRA enforces safety regulations, such as speed limits and requirements for safety features such as positive train control. Non-legislative recommendations for FRA policy come from the Rail Safety Advisory Committee, established in 1996, though much of FRA policy is created via congressional legislation; for example, the Rail Safety Improvement Act of 2008 was an act of Congress, to which the FRA enforced through a series of regulations published two years later. These regulations include enforcement of positive train control and enforcement of more stringent conductor certification requirements.

In 2011, the FRA began the process of updating its electronic device policy for active train operators.

List of administrators
Sarah Feinberg was the Administrator of the FRA from 2015 to 2017. Feinberg was the second woman to lead the agency. Her appointment was announced by United States Secretary of Transportation Anthony Foxx on January 12, 2015 and confirmed on October 28, 2015. Feinberg had previously served as Foxx's Chief of Staff, managing DOT's ten modal organizations, and spearheading its legislative, policy, and communications efforts. Feinberg's tenure as Administrator featured a greater emphasis on the enforcement of safety rules and regulations relative to her predecessors.

Joe Szabo was the first FRA Administrator to be chosen from the ranks of railroad employment. .

Patrick T. Warren, Executive Director of the FRA, is the current acting Administrator pending the appointment and confirmation of a new Administrator.