His last job before joining the Lions was as a member of the number two broadcast team for NFL on Fox,[3] and the color commentator for Monday Night Football on Westwood One.

It stood as the worst single-season record in NFL history until 2017, when it was tied by the 2017 Cleveland Browns who went winless in the season.

[7] Millen was recruited from Whitehall High School by Penn State, where he played for the Nittany Lions in the 1976, 1977, 1978, and 1979 seasons.

At Fox, Millen came to be considered the number-two analyst for its nationally broadcast games, behind John Madden (who had been teaming for years with Pat Summerall).

On June 15, 2009, Millen was named the lead analyst for the NFL Network's Thursday Night Football telecast, replacing Cris Collinsworth.

[11] He was also a color analyst for ESPN College Football telecasts, teaming with Sean McDonough, Joe Tessitore, and Bob Wischusen.

Since 2015, Millen has provided color commentary for college games on the Big Ten Network and occasionally for NFL on Fox.

In 2001, Millen left broadcasting to assume the job of the Detroit Lions' CEO and de facto general manager.

Detroit's .277 winning percentage was among the worst ever compiled by an NFL team over a seven-year period; only the Chicago Cardinals of 1939-1945 (10–61–3, .141)[13] and the Tampa Bay Buccaneers of 1983–1989 (26–86, .234) were less successful.

"[15] The Wall Street Journal said that NFL executives admit in private that Millen "has made more bad draft decisions than anyone else in two centuries.

[17] With a draft record that included a number of high first-round draft picks who were considered poor choices, including Charles Rogers, Joey Harrington, Mike Williams (chosen over DeMarcus Ware despite initial organizational agreement for Ware), and others,[18] and widespread disappointment among fans, the Detroit media, and even some players, Millen received a five-year contract extension from Ford at the start of the 2005 season.

[25][26] Former Pistons power forward Rasheed Wallace even took part in the chant during a late timeout in a December 16, 2005 game against the Chicago Bulls.

[26] A "Fire Millen" sign was shown in the background of a February 3, 2007 broadcast of ESPN College GameDay at the University of Kansas.

More "Fire Millen" chants were heard at wrestling events, including WWE's WrestleMania 23 at Ford Field and TNA's Bound for Glory.

[29] In a game against the Chicago Bears on December 24, 2006, another group of fans, led by Herbert Nicholl Jr., planned a walkout protest towards the end of the first half to express their disgust with Millen's management.

On the January 3, 2009, edition of NBC's Football Night in America, Millen admitted his role in the team's downfall, saying he would have fired himself after the 2008 season.

[40] The transplant surgery was performed successfully at Beth Israel Medical Center in Newark, New Jersey on Christmas Eve 2018.

[41] On January 5, 1986, at Los Angeles Memorial Coliseum, after losing the AFC divisional playoff game to the New England Patriots, Millen intervened in an on-field dispute between Raiders player and teammate Howie Long and Patriots general manager, Patrick Sullivan, by punching Sullivan in the face.

On April 24, 2010, at the 2010 NFL draft in Manhattan, Millen referred to fellow ESPN commentator Ron Jaworski as a "Polack," after which he made an on-air apology, stating that he "didn't mean anything" by the remark.