Education Secretary of Virginia
After Kaine's term as governor ended, Holton served as director of the Great Expectations program, an initiative that helped foster children attend schools in the Virginia Community College System. In 2014, Virginia governor-elect Terry McAuliffe appointed Holton to be the state's Education Secretary.
As Education Secretary, Holton wrote in 2015 that high-stakes testing in Virginia resulted in "teaching to the test" and made it difficult to attract good teachers to low-income schools. Holton supported increases in teacher pay and changes to the state's high school curriculum. She said she supported increased professional development for teachers. She also indicated her support for McAuliffe's 2016 legislative proposals to change high school graduation requirements and focus on early college courses and industry credentials. Holton resigned as Education Secretary on July 25, 2016, in order to focus on her husband's campaign for vice president.
In February 2017, Governor McAuliffe appointed Holton to the Virginia State Board of Education.
As a member of the Board of Education, Holton stated that she was in favor of charter schools along with other forms of education innovation, positing that strong charter school proposals help provide children with a pathway to life success. Holton also stated that Virginia's tradition of charter schools requiring approval by local school boards, as enshrined in the Constitution of Virginia, has served Virginia well, encouraging charter school proposals to make their case to local school boards.