Prior to the NFL, he was the head football coach at Hillsdale High School from 1960 to 1962, Napa Junior College in 1964, and UCLA from 1974 to 1975.

Vermeil's NFL tenure would see him improve the fortunes of teams that had a losing record before he arrived and bring them all to the playoffs by his third season, which included a Super Bowl title with the Rams.

Becoming Philadelphia's head coach in 1976, Vermeil took over for a team that had not qualified for the postseason, won a playoff game, or clinched their division since 1960.

Vermeil holds the distinction of being named Coach of the Year on the high school, junior college, collegiate, and professional levels.

He worked at his father's auto repair shop as a teenager and played at quarterback on the Calistoga High School football team.

[1] In his first head coaching position, Vermeil returned to Napa Junior College in 1964, leading the Chiefs to a 7–2 record, best in the school history.

[7] Vermeil began his NFL head coaching career in 1976 with the Philadelphia Eagles, taking over after the team went 4–10 the previous year.

[10] That 1978 season featured breakthrough years by NFL stars Ron Jaworski, Wilbert Montgomery, and one of the greatest games in Eagles history—the seminal Miracle at the Meadowlands.

In the 1980 season, Vermeil led the Eagles to Super Bowl XV after defeating the Dallas Cowboys for the NFC championship.

In actuality, Vermeil had seen tape of Papale playing semi-pro ball in Philadelphia and invited him to a workout and a subsequent tryout.

[15] Following the 1994 season, the Eagles fired Rich Kotite and owner Jeffrey Lurie inquired about bringing back Vermeil as coach.

Under Warner, the Rams offense exploded, and they finished the 1999 season with a record of 13–3 in one of the biggest single-year turnarounds in NFL history, ushering in the era of what would become known as "The Greatest Show on Turf".

Pro Bowl running back and team leader Priest Holmes suffered a season-ending injury against the San Diego Chargers in the eighth week of the season.

On December 31, Vermeil announced that he would retire at the conclusion of the 2005 season,[19] and the next day he led the Chiefs to a 37–3 rout over the Cincinnati Bengals.

When not in Kansas City, the entire Vermeil family enjoys spending time and working on "The Ranch", a 114-acre (0.46 km2) homestead located outside Philadelphia in rural Chester County, Pennsylvania.

Vermeil was actually once reprimanded by the NFL when during a game he promised kicker Morten Andersen a bottle of Cabernet Sauvignon if he could kick the game-winning field goal versus Oakland.

In the 2021 film American Underdog, Vermeil is portrayed by Dennis Quaid when he gave Kurt Warner an opportunity to play for the St. Louis Rams.

During his first retirement, Vermeil worked as a game analyst for both CBS (1983–87) and ABC Sports (1988–96), most of the time paired with Brent Musburger.

[24] Vermeil had a short cameo in the 2011 film The Greening of Whitney Brown, set in Chester County, in which he plays a football coach for the local middle school.

[25] The 2001 book autobiography Touched: The Jerry Sandusky Story (ISBN 9781582612706) includes a quote in a foreword[26] from Vermeil: "He could very well be the Will Rogers of the coaching profession.

A 2011 account about the book said "Sandusky paints a picture of himself as someone who would consistently take risks in pursuit of what he often refers to as 'mischief'" and there are many other citations and quotes which look "different in light of the horrendous allegations".

[28] After the firing of PSU president Graham B. Spanier, it was reported that Vermeil on November 8, 2011, "told [Philadelphia] Action News, 'I don't think there's anything that could discolor the quality of Joe Paterno's legacy.

'"[29] Vermeil also served on the Honorary Board of Sandusky's Second Mile children's foundation, along with Philadelphia Eagles coach Andy Reid, Matt Millen from ESPN, actor Mark Wahlberg and football player Franco Harris, among others.

[38] After John Madden passed on December 28, 2021, Vermeil became the oldest living coach of a Super Bowl winning team.