Cottrell began his coaching career at Rutgers University, where he worked as an assistant for eight years. In 1981, he got his first NFL coach job when Marv Levy hired him as linebackers coach for the Kansas City Chiefs.
Considered an innovator in the 3–4 defense, Cottrell was an assistant coach for the Buffalo Bills from 1995 to 2000, the last three seasons as defensive coordinator. From 1998 through 2000, the Bills finished no worse than sixth in the league in total defense. In 1999, the Bills led the league in total defense.
In 2001, he joined the New York Jets as assistant head coach and defensive coordinator, and operated the 4–3 scheme favored by head coach Herman Edwards. He stayed for three seasons.
In 2003, Cottrell was a finalist to become the head coach of the San Francisco 49ers.[1] He ultimately lost the job to Dennis Erickson.
Cottrell then spent two seasons (2004–2005) as defensive coordinator for the Minnesota Vikings. In 2005, the Vikings finished fifth in the NFL in takeaways and earned a postseason berth, and defeated the Green Bay Packers in a Wild Card contest. Cotrell was let go, along with Head Coach Mike Tice and the rest of his staff. Cottrell then announced his retirement.
In February 2007, he became the defensive coordinator under new Chargers head coach, Norv Turner. During the regular season, the Chargers led the NFL in takeaways (48), interceptions (30), and passing rating defense (70.0), the first time a Chargers team ever led in any of these categories. In 2008, many fans wanted Cottrell to be terminated.[citation needed] At the midpoint of the season, the team had a record of 3–5 despite having a highly effective offense. Many[weasel words] attributed this poor record to the fact that the Chargers ranked last among NFL teams in defending against the pass. Defenses led by Cottrell had similar problems in New York and Minnesota. At the midpoint of the 2008 season, the San Diego defense, generally considered to have fantastic talent,[weasel words] had gone two entire games without a quarterback sack nor a takeaway.
On October 28, 2008, Cottrell was fired from his position as San Diego's defensive coordinator.[2]