John Ashcroft was born in Chicago, Illinois, on May 9, 1942, but grew up in Springfield, Missouri. He graduated from Springfield's Hillcrest High School in 1960 and concluded his studies at Yale University in 1964. He then returned to Chicago, earning his J.D. from the University of Chicago Law School in 1967.

After finishing his legal studies, Ashcroft began teaching at Southwest Missouri State University until running for Congress in 1972. In 1974, Ashcroft became an assistant to Missouri's attorney general, a position he himself was elected to in 1976. In 1984, he became governor of Missouri, serving for two terms as the state's top public official. Ashcroft was elected chairman of the National Governors Association in 1991. His popularity as governor provided him with the momentum for a successful Senate campaign in 1994. Ashcroft lost his bid for reelection in 2000 but was chosen by President George W. Bush to serve as attorney general.

John Ashcroft announced his resignation after the 2004 election. Bush nominated Alberto Gonzales to succeed him. The Senate confirmed Gonzales in February 2005.