After spending two seasons as an assistant coach with the Boston Patriots of the brand newAFL, Collier joined the Buffalo Bills in 1962 as a defensive coach. The team won the 1965 AFL Championship Game over the San Diego Chargers with help from defensive alignments that Collier designed. One idea he came up with was similar to the modern zone blitz; Collier's defense featured defensive line players moving back to cover pass attempts. Collier was promoted to head coach in 1966, after previous coach Lou Saban resigned. The Bills' best season under Collier came in his first year, when they won the Eastern Division with a 9–4–1 record, eventually losing to the Kansas City Chiefs in the AFL Championship Game. After coming within one game of an AFL championship, the team slumped to 4–10 in 1967. After a poor performance by the Bills in a 1968 pre-season game, Collier set up a scrimmage for his team. During the practice session, quarterbackJack Kemp broke his right leg, an injury that forced him to undergo season-ending surgery. The Bills fired Collier after a 48–6 loss to the Oakland Raiders in the second week of the regular season. Sports Illustrated opined that "Collier's fate undoubtedly was decided..." by Kemp's injury.
Following his time as head coach of the Bills, Collier became a Denver Broncos coach in 1969 and spent 20 years with the team, who reached three Super Bowls with him as defensive coordinator. Collier was the architect of the Broncos' 3–4 defense in the late 1970s, a scheme that was known as the Orange Crush Defense. Although he preferred to set up the Broncos' defense with four linemen, Collier occasionally organized a 3–4 defense experimentally. After an injury to Lyle Alzado early in the 1976 season, Collier used the system more regularly and improved upon it: author Terry Frei called him "the scientist in the laboratory, coming up with ways to make the defense even better." After being hired by Saban, he remained the defensive coordinator for four subsequent Broncos head coaches. Dan Reeves fired Collier after the 1988 NFL season.
From 1991 to 1992, he was defensive coordinator for the New England Patriots. Collier took over a Patriots defense that had given up the second-most points in the league during a 1–15 season in 1990. However, Collier's first year saw the Patriots defense improve from second-worst in the league to the middle of the pack. Helping the Patriots' improved rankings was the fact that their run defense, which was last in the league in 1990, improved to 9th in the league in 1991. The Patriots failed to build on their 1991 defensive performance, as the unit finished 23rd overall during the 1992 season. New England ended up 2–14, winning four fewer games than they had in 1991. After his stint with the Patriots ended, Collier retired from the NFL.
