He has been the head coach of five collegiate football programs and two NFL franchises. He is currently the head coach of the Idaho Vandals of the Western Athletic Conference (WAC), a team he had coached over twenty years earlier.

Erickson was raised in Everett, twenty five miles north of Seattle. His father, "Pinky", was a high school head football coach at Cascade High School. The younger Erickson played quarterback at the rival high school (Everett HS), coached by next-door neighbor, Bill Dunn. This "made for some quiet dinners on game day." As a junior, Dennis was the starting quarterback, beating out the former starter, senior Mike Price, another future college head coach. Price, the son of the head coach of Everett Junior College, was moved to defense (as a safety). When Erickson left Washington State in 1989, he recommended Mike Price as his replacement, who got the job, and rented Erickson's Pullman home. Erickson had beaten out Price for the job in 1987. Six years earlier in 1981, Price had beaten Erickson out for the job at Weber State in Ogden, Utah. While at Idaho, Erickson was 2-2 vs. Price's Weber teams. At Oregon State, Erickson was 2-1 against Price's Washington State teams, not playing in 2002.

In 1965, Erickson graduated from high school and accepted a football scholarship to Montana State in Bozeman. He was an effective undersized quarterback (quick feet, marginal arm) from 1966-68, earning all-conference honors (Big Sky). Immediately after his senior season, he began his coaching career as a graduate assistant for the Bobcats in 1969. In 1970, at age 23, Erickson became the head coach at Billings Central High School, staying for just a single season. From 1971 through 1981, he was a collegiate assistant coach (offense) at Montana State (3 yrs.), Idaho (2), Fresno State (3), & San Jose State (3).

Erickson's head coaching career began in December 1981, at age 34, when he was hired at Idaho (following a successful stint as Jack Elway's offensive coordinator at San Jose State). Building on his reputation as an offensive innovator, Erickson became Idaho's all-time winningest head coach in just four seasons with the Vandals (1982-85). He took his "spread offense" with him to Division I-A Wyoming in 1986 for a single season, returned to the Palouse with Washington State of the Pac-10 for two (1987-88), then on to the University of Miami (1989-94) for six, winning two national championships. He was then hired as an NFL head coach, staying with the Seattle Seahawks for four seasons (1995-98) before being fired, then went back to the college level with Oregon State in 1999 for four more. He chose to return to the NFL with the San Francisco 49ers and lasted just two seasons (2003-04) before being relieved. He did not coach during the 2005 season.

On February 8, 2006, the University of Idaho announced the re-hiring of Dennis Erickson as its head football coach. Erickson won 32 games in his four seasons as the Vandals' head coach (1982-1985), then a Division I-AA program in the Big Sky Conference. Idaho moved up to Division I-A in 1996.