Taken in the third round of the 1969 AFL-NFL Draft out of Maryland State (now UMES), Billy Thompson made an immediate, multi-dimensional splash as a rookie. Deployed as a right cornerback and return specialist, Thompson put together an electric debut campaign, becoming the first player in professional football history to lead his league in both kickoff return average (28.5 yards) and punt return average (11.5 yards) in the same season.

Though Thompson was initially a dangerous special teams player, he became a franchise cornerstone after head coach John Ralston moved him from cornerback to strong safety in 1973. This switch unlocked his full potential, allowing him to serve as the tough, ball-hawking key figure of the secondary. He anchored Joe Collier's renowned "Orange Crush" defense, known for disciplined tackling, relentless pursuit, and frequent turnovers.

Thompson's best season was during Denver's storybook 1977 campaign. Snaring five interceptions, recovering three fumbles, and spearheading a defense that powered the Broncos to their first AFC championship and Super Bowl XII appearance, Thompson was named a First-Team All-Pro and earned his first Pro Bowl selection. He added back-to-back Pro Bowl nods in 1978 and 1981, routinely jump-starting the offense by converting opponent mistakes into instant points. In fact, Thompson scored seven career defensive touchdowns—three on interception returns and four on fumble recoveries—the latter standing as an NFL record for decades.

Beyond his playmaking prowess, Thompson was an absolute ironman. He started 178 of his 179 games in Denver, setting a franchise record with 142 consecutive starts that stood for years. A long-time team captain, he retired following the 1981 season as the first player in franchise history to log 13 active seasons in a Broncos uniform.

With Denver, he compiled 40 interceptions for a franchise-record 784 return yards, 21 fumble recoveries, and seven defensive touchdowns, while adding 2,970 combined return yards and was inducted into the Denver Broncos Ring of Fame in 1987 as the sole member of his class.