White worked for a church in Birmingham before joining the British civil service in 1989. She worked first at the Treasury and later for the British Embassy in Washington, which was where she met her husband Robert Chote. She also worked at the 10 Downing Street policy unit during the Blair government, at the World Bank, and as a director general at the Department for International Development in 2003–09 and then at the Ministry of Justice in 2009–11, and also at the Department for Work and Pensions. At the Treasury, she supervised a review of the financial management of government and the Treasury's management response to the international financial crisis of 2007–08. She was Director General for Public Spending at the Treasury from 2012 to 2013, and then replaced Tom Scholar as Second Permanent Secretary in 2013. She was the first black person to become a Permanent Secretary at the Treasury, and the second woman after Dame Anne Mueller in the 1980s. In November 2014, The Voice named White the 7th most powerful black person in Britain. White has been recognised for her influence as one of the most powerful Black British people in the UK on a number of occasions by Powerlist, regularly ranking in the top 10 since the 2016 list including second place in 2019 In December 2014, it was announced that White would be the chief executive of Ofcom from March 2015, replacing Ed Richards as the previous chief executive and Steve Unger as the interim chief executive. In June 2019, it was announced that White would be stepping down from her role at Ofcom to replace Sir Charlie Mayfield as the sixth Chairman of the John Lewis Partnership. White succeeded Mayfield during a meeting of the John Lewis Partnership Council on 4 February 2020. It was confirmed that White will be awarded an annual salary of £990,000 for her role at the John Lewis Partnership, a significant increase on her previous salary, which was £341,700 according to data released by Ofcom. White was appointed Dame Commander of the Order of the British Empire in the 2020 New Year Honours for public service.
White married the economist Robert Chote at the British Embassy in Washington, DC, in 1997, when she was working at the British embassy and Chote was working for the International Monetary Fund. Chote has been the chairman of the Office of Budget Responsibility since 2010. The media have dubbed the couple "Mr and Mrs Treasury". They have two children.