He emerged as a figurehead for San Francisco’s large gay community, and was known as the “Mayor of Castro Street”, a title which he himself coined. With each campaign, he garnered a larger number of supporters. Milk was successful in reaching out and making alliances among the city’s ethnic populations and among labor union leaders, but not among the rank and file members. Milk’s opponent in the 1976 race for the California State Assembly was Art Agnos, who would win the seat by 3,600 votes out of 33,000 ballots cast.In 1976 San Francisco voters voted to replace city-wide elections with district elections, effective in the 1977 city elections. This switch to district elections ushered in the most diverse Board of Supervisors the city had ever seen. Milk was the first openly gay elected official of any large city in the United States, and only the third openly gay elected official in all of the US, after Kathy Kozachenko and Elaine Noble. Milk represented District 5, which included the Castro.

The diverse board included the former police officer and firefighter Dan White as well as the gay and liberal Milk. White had to resign from being a firefighter as San Francisco charter barred people from holding two city jobs at the same time so he took up a second job to supplement the pay downgrade, running a restaurant business, which failed. White, a Roman Catholic[2] and outspoken anti-gay conservative, who was elected with strong support from the city’s police union in part to fight “official tolerance of crime and of overt homosexuality” was counterpoint to Milk, an outspoken liberal who “frequently opposed him on the board.”

Milk became highly visible in the media debating California Senator John Briggs throughout the state on Proposition 6, The Briggs Initiative, to “prohibit homosexuals from teaching in California public schools,” a topic on which White and Milk “were sharply divided” because it would have empowered California school boards to fire teachers that “practiced, advocated, or indicated an acceptance of homosexuality.”