In the summer of 2004, Stoney served as a Governor's Fellow in Mark Warner's administration. Stoney then worked as an organizer in John Kerry's 2004 presidential campaign as well as for the Democratic National Committee and the Democratic Party of Wisconsin in a get out the vote effort. Five of his colleagues were later charged with slashing the tires of a van meant to be used to drive Republican voters to the polls. Stoney initially lied to police claiming he had no knowledge about the incident. He later admitted to FBI investigators that he was present in the Democratic campaign offices after his colleagues came in to brag about slashing the tires. Stoney then went on to testify against his colleagues and fully cooperated with law enforcement. After questioning during a committee meeting with Virginia Republican lawmakers about his indiscretion, it was accepted as "an isolated, youthful mistake." During the 2005 Virginia Attorney General election Stoney worked for Creigh Deeds, who narrowly lost. Stoney then worked for the Democratic Party of Virginia from 2006 to 2009, first as political director and then executive director. In this role, he worked extensively with President Barack Obama's successful 2008 presidential campaign. In 2011, after losing his father, who had supported his political involvement, Stoney began working as a consultant at Green Tech, an automotive company run by Terry McAuliffe. The following year Stoney began working with McAuliffe's 2013 gubernatorial campaign, as deputy campaign manager, under campaign manager Robby Mook. When McAuliffe won, Stoney became deputy director of the gubernatorial transition team, during which McAuliffe described Stoney as his "closest adviser." McAuliffe appointed Stoney as Secretary of the Commonwealth of Virginia on November 18, 2013. Following confirmation by the Virginia General Assembly, he took office on January 17, 2014. As Secretary of the Commonwealth, Stoney championed efforts for the restoration of voting rights for felons who have completed their sentences, an effort begun under Governor Bob McDonnell and accelerated under Governor McAuliffe. Stoney said that "once you have served your time and paid your due, we still should not be punishing you years afterwards. Instead, we should find ways to give that individual an opportunity to better themselves and to contribute to society."
Mayor of Richmond
could not run for re-election as mayor of Richmond because of a two-term limit. Stoney became a candidate in the 2016 election to succeed him, announcing his candidacy after resigning as Secretary of the Commonwealth. Stoney won the election over Jack Berry, 36% to 34%, with Joe Morrissey in third place. Shortly after the election, Mayor-elect Stoney named Tiffany Jana and Bill Leighty as co-chairs of his transition team, with University of Richmond professor Thad Williamson named as director. Stoney was sworn into office on December 31, 2016. At 35 years of age, he became Richmond's youngest elected mayor. In March 2019 Mayor Stoney proposed a nine-cent per $100 assessed value real estate tax hike. He also proposed adding a 50-cent tax on packages of cigarettes.