Ashcroft was born in Chicago, Illinois where his family had moved to be nearer to the world headquarters of the Assemblies of God church, part of the Pentecostal fundamentalist movement. He was educated in Springfield, Missouri and at Yale University, where he graduated in 1964. He received a J.D degree from the University of Chicago in 1967 and briefly taught business law at Southwest Missouri State University.
He began his career in Missouri government in 1973. He was Governor of Missouri from 1984 to 1993. He was elected to the Senate from Missouri in 1994. He ran for re-election in 2000 against then-Governor Mel Carnahan, who died in an airplane crash about two weeks prior to the election. Due to Missouri state election laws, Mel Carnahan's name could not be removed from the ballot and his wife, Jean Carnahan, announced she would serve in his place if he was elected. Carnahan posthumously won the election, and it was widely reported that John Ashcroft was defeated by "a dead man," as Mel Carnahan's name remained on the ballot. Others contend, however, that Jean Carnahan may have won the election due to the "sympathy vote" for her late husband. Despite his defeat, Ashcroft was subsequently nominated as Attorney General by George W. Bush in December 2000. Despite a contentious nomination process, he was confirmed by the Senate.
Ashcroft is considered a leading member of the Christian right wing of the Republican party and is one of the highest-ranking representatives of the group in the Bush Administration. As a devout Pentecostalist, he shuns such activities as dancing and alcohol consumption. Ashcroft's religious beliefs have led commentators, including Senator Charles Schumer, to question whether he could effectively enforce certain laws, especially those pertaining to abortion. Ashcroft has maintained that he will enforce laws whether he agrees with them or not.
In July of 2002 Ashcroft suggested the creation of Operation TIPS, a proposed domestic program in which government employees would inform on suspicious behavior they encounter while performing their duties. The program was criticized in the media as an encroachment on the first and fourth amendment; and in fact the United States Postal Service balked at the suggestion, refusing outright to participate. Ashcroft defended the program as a necessary component to the ongoing war on terrorism but the proposal was eventually abandoned.
Ashcroft's opponents have accused him of unnecessarily using the spectre of terrorism as justification for restricting civil liberties. A few have even coined the pejorative term Ashcroftism to refer to a set of ideas or policies alleged to be similar to those of Ashcroft.
The former senator famously once boasted of his conservatism, saying there are two things you find in the middle of the road: "a moderate and a dead skunk", adding he did not want to be either.