In 2008, Sullivan was an advisor to Hillary Clinton during the primary cycle and then to Barack Obama during the general election campaign. He prepared Clinton and Obama for debates. When Clinton became secretary of state, Sullivan joined as her deputy chief of staff and director of policy planning, and he travelled with her to 112 countries.
Sullivan worked in the Obama administration as deputy assistant to the president and national security advisor to Vice PresidentJoe Biden. He became Biden's top security aide in February 2013 after Clinton stepped down as secretary of state. In those posts, he played a role in shaping U.S. foreign policy towards Libya, Syria, and Myanmar.
He was reported to be the only senior staffer who repeatedly suggested that Clinton should spend more time in Midwesternswing states during the election campaign. Clinton's surprising failure to win those states was a key factor in her defeat. Sullivan was prominent in many of the Podesta emails released by WikiLeaks during the 2016 US presidential election, including Sullivan questioning if Democratic primary candidate Martin O'Malley's 100% clean energy by 2050 plan was "realistic". After the election, he confessed to feeling "a keen sense of responsibility" for Clinton's defeat. On March 24, 2022, former President Donald Trump sued numerous people including Hillary Clinton and Jake Sullivan alleging a conspiracy by the Hillary Clinton campaign to invent the Russian collusion scandal. The suit was dismissed on September 8, 2022, and on January 19, 2023, a federal judge imposed nearly $1 million in sanctions on Trump and his lawyer Alina Habba, calling the suit “completely frivolous.”