After college, Collinsworth was drafted by the National Football League's Cincinnati Bengals in the second round of the 1981 NFL Draft.
In Super Bowl XVI, Collinsworth (Cincinnati Bengals) caught four passes for 107 yards, but committed a costly fumble when he was hit by San Francisco defensive back Eric Wright.
In 1985, Collinsworth signed with the Tampa Bay Bandits of the United States Football League, but the contract was voided when he failed the physical due to a bad ankle. He returned to the Bengals and played for them until the end of the 1988 season, catching 3 passes for 40 yards in Super Bowl XXIII, the final game of his career. He finished his 8-season career with 417 receptions for 6,698 yards and 36 touchdowns in 107 games.
Collinsworth was named Anthony Cris instead of "Cris Anthony" by his mother because, according to her, it "sounded too much like chrysanthemum.
In 1990, he became a part of the NBC network's NFL broadcasts, as well as some of the college programming. He joined the NBC pregame show in 1996.
In 1998, Collinsworth joined the NFL on FOX team after NBC lost their broadcast rights to CBS. After several years as a color commentator on the FOX NFL Sunday pregame show, Collinsworth was assigned to the network's lead game broadcasting crew (teaming with Joe Buck and Troy Aikman) in 2002. He worked on Fox's Super Bowl XXXIX telecast three years later.
Collinsworth was also the host of the television show Guinness World Records Primetime during his stay at Fox.
In 2006, Collinsworth could be seen on three networks during football season. In addition to co-hosting Inside the NFL on HBO, he returned to NBC as a studio analyst for that network's Sunday night NFL coverage and does color commentary on the NFL Network.
He also served as color commentator for NFL Network Thursday night games (and one Saturday-night game) alongside play-by-play man Bryant Gumbel. In 2007, Collinsworth was the Studio Analyst on NBC's Notre Dame Football package.
Collinsworth was recently announced as the color commentator on Madden NFL 09 along with Tom Hammond. He received a Sports Emmy Award in April 1998 as "Outstanding Studio Analyst" and his second in 1999. He was also recognized with his third and fourth Sports Emmy Awards in 2003 and 2004 as "Outstanding Sports Personality/Studio Analyst." In May 2006 he added a fifth with an Emmy Award again in the category "Outstanding Sports Personality/Studio Analyst" for his work on HBO. Collinsworth was serving as a correspondent for NBC Sports coverage of the 2008 Summer Olympics.