From 1998 through January 2007, Dudley worked at the non-profit Mercatus Center at George Mason University, where she directed the Regulatory Studies Program from 2003 to 2006. As an adjunct professor at the George Mason University School of Law from 2002 to 2006, she designed and taught courses on regulations and led regulatory clinics. Earlier in her career, Dudley served as a career civil servant, working as a policy analyst at the Environmental Protection Agency (1984-1985), an economist at OIRA (1985 – 1989), and an economist advisor at the Commodity Futures Trading Commission (1989 - 1991). From 1991 until 1998, she was Vice President and Director of Environmental Analysis at Economists Incorporated, a consulting firm.