After playing one season for the Titans, he injured his posterior cruciate ligament, and returned to MSU to obtain a Master's degree. He became an assistant coach at MSU in 1963. He then coached high school football and basketball at Bay City, Michigan's Visitation HS for two years losing only two games in his first year in 1964, and his team was undefeated in his second year in 1965, winning their league championship. He later left for the University of Dayton to serve under head coach John McVay. He also served as an assistant coach at the University of Iowa and Southern California. He ultimately developed a close relationship with John McKay after working under his wing at USC, and went on to work as the defensive coordinator and defensive backs coach of the Tampa Bay Buccaneers from 1982–1984.
After 13 seasons as an assistant in the NFL, Fontes took over the Lions as interim head coach in mid-season of 1988 after head coach Darryl Rogers was fired. Fontes was regarded as somewhat of an up-and-comer in NFL coaching circles during his time in Tampa Bay as defensive backs coach under John McKay, and became a highly regarded ball skill and positioning educator for defensive backs in the "3-4" defense.
The Lions would go on to achieve some success during his tenure. The team made the playoffs in 1991, 1993, 1994, and 1995 under his leadership. Fontes coached the 1991 and 1993 squads that won the NFC Central Division Title. The 1991 team won 12 regular season games (a franchise record), and Fontes earned NFL Coach of the Year honors through the Associated Press and United Press International. The Lions lost in the 1991 NFC Championship game to the Washington Redskins. Detroit was unable to find success in the post-season during his tenure which ultimately resulted in his termination.
Fontes' ability to survive rumors of being fired earned him nicknames like "Big Buck" (stemming from a comparison he made between his job security and a hunted buck deer) and "Rasputin" (coined by Chris Berman due to Fontes' apparent ability to "miraculously" coax a winning streak out of his team every time he was about to be fired). Berman also referred to him as the "Nanook of the North" because of Fontes' desire to bundle up so heavily in the winter cold. He has also been referred to as "Mr. Snuffleupagus", due to his resemblance of the "Sesame Street" character of the same name. Fontes was also the brunt of many media jokes. Jokes like "Mr. Fontes is an expert in primary colors and beige" reflect the lack of respect that haunted his tenure.
Fontes was regarded as very personable, often joking with the media about his precarious job situation. He drew the line for this comedy though after the Detroit Free Press ridiculed him for sporting Mickey Mouse ears at a Disney charity. The Free Press ran a tongue-in-cheek multiple choice quiz as to why he was wearing them the following day. The offbeat answers ranged from "Wearing his thinking cap" to "President of the Mouse Davis fan club". An irate Fontes slammed the media for making such a personal attack against him in such bad taste. He said, "It ain't funny....if you don't like me, tell me. That's bull. Didn't like it at all. I did something for charity and for kids, and I'll keep doing things for charity and for kids." This strong sense of compassion and sacrifice for others is probably what endeared players to him. The players responded to Fontes and always came to his defense when the coach fell into the "firing line".
Fontes popularity was waning in the later years of his career with the Lions. Many local media outlets and fans were openly critical of Fontes, correctly noting he amassed the most losses of any coach in Lions' history and overall record was under .500. The desolate years of mediocrity prior to Fontes seemed to be an afterthought, as was Fontes' role as a long time assistant in that mediocrity. Many felt the Lions were underachieving and that a change in leadership to a firm disciplinarian, such as Bobby Ross, would produce better results. The move backfired as Ross was never able to build a strong relationship with superstar running back Barry Sanders. It's widely speculated that the hiring of Ross accelerated the retirement of Sanders, who was very close with Fontes. In ESPN's SportsCentury video on Barry Sanders, Barry's father confirms that Barry contemplated retiring before the start of the 1997 season, which was to be Ross' first season as Lions coach. In his autobiography, "Now you see him", Barry says of Wayne Fontes: "I thought he deserved another chance." (ISBN 1-57860-139-8 p. 97)
As of 2018, Fontes is the only Lions coach to lead the team to a NFC championship game (versus the Washington Redskins following the 1991 season). He led them to the playoffs in four out of eight seasons while he was head coach, including three consecutive playoff berths (1993, 1994, and 1995). He left the Lions compiling the most wins in franchise history (67), most playoff appearances (5), most losses (71), and is 9th (out of 23 coaches) in total win percentage.
Some rumors indicate that Fontes drafted Barry Sanders in 1989 against the wishes of other members of the Lions staff, and accounts from some contemporaries do indicate that Fontes was definitely focused on acquiring Sanders. Barry Sanders made a point to thank Fontes for his guidance in his Pro Football Hall of Fame induction speech. The mutual admiration and respect between Fontes and Sanders was very strong and transcended beyond the football field. Toward the end of his time in Detroit, an anti-Fontes sentiment grew among some Lions team members, but Sanders remained a staunch supporter of the coach. Of Fontes, Sanders said: "He proves that a coach can show affection and appreciation and still win." Sanders, to this day, credits Fontes for making him a superstar running back.
Fontes still supports local Detroit charities on occasion with his former players although those opportunities have been fewer as of late. After serving briefly as a color commentator on the English-language broadcasts of NFL Europe games, Fontes retired to his home in Tarpon Springs, Florida. He is frequently spotted at Tampa Bay Buccaneers games where he maintains a strong friendship with Jim Gruden, father of former Buccaneers Head Coach Jon Gruden.