Burton earned a BA degree in social science in 1954 from San Francisco State University and was the University's Alumnus of the Year in 1998. From 1998 until he was forced out of office by term limits in 2004, he served as the President pro tempore of the State Senate. Prior to his time in the Senate, he served in the California State Assembly from 1965-74, and again from 1988-96. He was originally elected to the Assembly to succeed his brother, Phillip, who had been elected to Congress. Burton was returned to the Assembly in a 1988 special election to succeed Art Agnos, who had been elected Mayor of San Francisco. Burton also served in the U.S. House of Representatives, alongside his brother, from 1974-82, when he resigned. As a legislator, Burton was known for expanding the scholarship program, and passing a law that would have required California businesses to pay for health coverage for their workers. The magazine California Journal said about Burton's departure from the Senate in 2005: "Gone will be the Senate's most vehement partisan for social services for the poor, the Senate's angriest voice against tax breaks for businesses and the wealthy, its loudest voice for protection of workers, its fiercest pro-labor advocate and its disciplinarian." After leaving the Senate, Burton formed the , an organization that, according to its web site, is "dedicated to improving the quality of life for California’s homeless children and developing policy solutions to prevent homelessness." In February 2007 he was appointed board member of the University of Phoenix. On April 26, 2009, Burton was elected chair of the California Democratic Party, succeeding Arthur Torres. He received roughly 76% of the vote, over his sole challenger, Chris Finnie of Santa Cruz. Burton stepped down as Chairman of the California Democratic Party in May 2017. He was succeeded by Vice Chairman Eric Bauman. At his farewell, he was reported to have punctuated his comments with profanity-laced tirades on President Donald Trump and others in front of such influential lawmakers as Nancy Pelosi, Kamala Harris, Tom Perez, and Gavin Newsom.
In 2008, Burton settled a $10 million sexual harassment lawsuit filed by Kathleen Driscoll, then the executive director of his charitable foundation for homeless children. She claimed Burton sexually harassed her by making unwanted advances, using suggestive language and commenting on her body. At a 2008 news conference in her attorney's office, Driscoll said, "I had a dream of helping homeless children through a job I loved. John Burton turned that dream into a sexual harassment nightmare and quite frankly a living hell."
