In 1978, disgruntled White resigned from the Board of Supervisors, frustrated by the low salary - $9,600 a year - then paid to members of the board. Soon he had a change of heart and asked popular Mayor George Moscone to reappoint him to the position. Moscone said no. On the evening of November 27, White entered City Hall through a window on the lower level, north. (At the time, this area was a supervisors' parking area. Today, the window that White entered is now a door.) White, a former policeman and fireman, shot and killed Moscone and gay Supervisor Harvey Milk. San Franciscans were indescribably shocked when Board President Dianne Feinstein announced that the mayor and Milk had been killed and Dan White was the suspect. Feinstein was sworn in as the new mayor as the entire City mourned for leaders Moscone and Milk. On May 21 the following year, White was convicted of voluntary manslaughter. The jury accepted a diminished capacity defense based on testimony that White was suffering from untreated depression. In doing so, the jury rejected first degree murder charges. The so-called Twinkie defense is a widely accepted misinterpretation of White's diminished capacity argument. Even the San Francisco Chronicle reported that White claimed his mind was fogged by too much sugar on the night of the murders. In reality, White's new found junk food habit was offered as evidence of his depression, not as the cause of it. Outraged San Franciscans responded to the court's decision to slap White on the wrist for killings (7 year sentence) by rioting at City Hall, the "White Night Riot." White was paroled in 1984 after serving just five years and a little more than a month behind bars at Soledad Prison. In 1985 he returned to San Francisco despite a request by Feinstein for White, the most reviled man in the City's history, to stay away.

Unable to make a new life for himself nor to escape the impact of his crimes, White attached a garden hose to the exhaust pipe of the family car, a yellow 1970 Buick Le Sabre and took his life on the morning of October 21, 1985. White, who left suicide notes to members of his family, died clutching family photos. An Irish ballad, "The Town I Loved So Well," sounded from a cassette player inside the Le Sabre as White filled the car with carbon monoxide. The body was discovered by White's brother, Tom, at White's 150 Shawnee Avenue residence shortly before 2 p.m. the same day.