After graduating from the New York State College for Teachers in Albany (1951), Milk served in the U.S. Navy during the Korean War and was discharged in 1955 (Milk later said that he was dishonourably discharged due to his homosexuality, but military records do not support this claim). He held several jobs before becoming a financial analyst in New York. In 1972 he moved to San Francisco, where he opened a camera store and soon gained a following as a leader in the gay community. His popularity grew when he challenged the city's gay leadership, which he thought was too conservative in its attempts to gain greater political rights for homosexuals.

In 1973 Milk ran for a seat on the city's Board of Supervisors but was defeated. After another unsuccessful bid in 1976, he was elected in 1977, becoming one of the first openly gay elected officials in U.S. history. The following year Milk and the city's mayor, George Moscone, were shot and killed in City Hall by Dan White, a conservative former city supervisor. At White's murder trial, his attorneys argued that his judgment had been impaired by eating junk food (a tactic later derided as the “Twinkie defense”); his conviction of the lesser charge of voluntary manslaughter sparked an uproar in the city that was subsequently termed the “White Night Riot.” Numerous books and films were made about Milk, including the 1984 documentary The Times of Harvey Milk, which earned an Academy Award; an opera, Harvey Milk (1995); and Milk (2008), a cinematic depiction of his political career that starred Sean Penn (Penn, Sean).