John Herrington was born in Los Angeles, California, on May 31, 1939. He earned his A.B. at Stanford University (1961) and his J.D. and LL.B. at the University of California School of Law (1964). Herrington practiced private law as an attorney (1965-1981) and had worked as deputy district attorney of Ventura County. Herrington was assistant secretary of the Navy from 1981 to 1983.

He began his work in the Reagan administration as deputy assistant for presidential personnel, holding that post from 1983 to 1985, serving next as secretary of energy from 1985 to 1989. Thereafter, he worked in California Republican politics, serving for a time as chairman of the state's Republican Party.