Singleton has been a leader in government relations and public policy law for over 20 years, having held several senior positions at the national level. Notably, she was senior counsel to the U.S. House of Representatives Committee on the Budget under former Congressman William H. Gray.

Singleton represents companies and trade associations throughout a wide range of industries in government relations matters related to international trade, transportation, energy and healthcare.

During her time on Capitol Hill, Singleton developed an extensive background in international development. She helped draft legislation that created the African Development Foundation (USADF); a government agency that supports African-led development and community growth through the provision of seed capital and technical support. She went on to serve as an advisory board member of USADF for 10 years. In 1996, then President, Bill Clinton, appointed Singleton as General Counsel of the United States Agency for International Development. During her five-year tenure, she was the chief legal advisor to 72 U.S. missions around the world.

Singleton has been on the Board of Directors of public utility holding company, Alliant Energy since 2001. She has served on the Board of United Rentals, the largest equipment rental company in the world, since 2004. Singleton also began a gubernatorial appointment as Secretary to the Commonwealth of Virginia State Board of Elections in 2015.