Dingell attended Capitol Page School in Washington, D.C. as well as Georgetown Preparatory School (in Garrett Park, Maryland) and was a page for the U.S. House of Representatives from 1938 to 1943. In 1944, at the age of 18, Dingell joined the United States Army. He rose to the rank of Second Lieutenant and received orders to take part in the first wave of a planned invasion of Japan in November of 1945; the Congressman has said President Truman's decision to use the atomic bomb to end the war 'saved' his life. He then attended Georgetown University in Washington, D.C., where he graduated in law in 1952. He was a lawyer in private practice, a research assistant to U.S. Circuit Court judge Theodore Levin, a Congressional employee, a forest ranger, and assistant prosecuting attorney for Wayne County until 1955, when John, Sr. died and John, Jr. won a special election to succeed him. He won the seat in his own right in 1956 and has been reelected 25 times. His district was called the 15th District from 1955 to 1965, the 16th District from 1965 to 2003, and the 15th District again since 2003. From 1981 until the Democrats lost control of the House in 1995, Dingell chaired the Energy and Commerce Committee and was regarded by analysts as one of the four or five most powerful members of the House. He is still the committee's ranking Democrat.

Dingell has always won reelection by double-digit margins, although the increasing conservatism of the white suburbs of Detroit since the 1970s led to several serious Republican challenges in the 1990s. However, he has won his last two elections with over 70 percent of the vote. With the retirement of Jamie L. Whitten at the start of a new Congress in January 1995, he became the longest-serving member in Congress. He is one of three people to serve in the House for 50 years, the others being Whitten and Carl Vinson. On Valentine's Day, 2006, Dingell became the second-longest serving member of the House, surpassing Vinson. If he is still serving in 2009, he will surpass Whitten's record for tenure in the House.

In 2002 he successfully defeated a challenge in the Democratic primary election from a slightly more liberal Democrat, Lynn Rivers, after redistricting by the Republican-controlled Michigan Legislature following the United States 2000 Census resulted in the two Democratic incumbents being placed into the same district; since that time, he has represented the liberal college towns of Ann Arbor and Ypsilanti.

Dingell is generally classed as a liberal Democrat, and throughout his career he has been a leading congressional supporter of organized labor, of social welfare measures and of traditional progressive policies. At the beginning of every Congress, Dingell introduces a bill providing for a national health insurance system, the same bill that his father proposed while he was in Congress. However, he was a strong proponent of Bill Clinton's managed-care proposal early in his administration.

On some issues, though, he reflects the conservative values of his largely Catholic and working-class district. He was a supporter of the Vietnam War until 1971. Although he supported the Johnson Administration's civil rights bills, he opposed campaigns to expand school desegregation to the Detroit suburbs via mandatory busing. He takes a moderately conservative position on abortion. He has voted against clean air bills if these appear to threaten Detroit's automobile industry. An avid sportsman and hunter, he strongly opposes gun control, and is a former board member of the National Rifle Association. For many years, Dingell has received an A+ rating from the NRA.

The political analyst Michael Barone wrote of Dingell in 2002:

"There is something grand about the range of Dingell's experience and about his adherence to his philosophy over a very long career. He is an old-fashioned social Democrat who knows that most voters don't agree with his goals of a single-payer national health insurance plan but presses forward toward that goal as far as he can. "It's hard to believe that there was once no Social Security or Medicare," he says. "The Dingell family helped change that. My father worked on Social Security and for national health insurance, and I sat in the chair and presided over the House as Medicare passed (in 1965). I went with Lyndon Johnson for the signing of Medicare at the Harry S. Truman Library, and I have successfully fought efforts to privatize Social Security and Medicare." Whether you agree or disagree, the social democratic tradition is one of the great traditions in our history, and John Dingell has fought for it for a very long time." On December 13, 2005, Dingell was honored at the White House with a Presidential lunch for his 50th anniversary. On December 15, 2005, Rep. Dingell read on the floor of the House a poem sharply critical of, among other things, Fox News, Bill O'Reilly and the so-called "War on Christmas".