While attending the University of Southern California, Morton played for the USC Trojans football team from 1990 to 1993. He broke twelve USC team and Pacific-10 Conference records for receptions and receiving yards. Morton was nicknamed "Big Play Morton" by Tom Kelly, and "Johnnie Hero" by USC broadcaster Pete Arbogast, thanks to a game-winning touchdown pass Morton caught in the 1990 USC-UCLA rivalry game—a 23-yard strike from Trojans quarterback Todd Marinovich with 16 seconds left that gave the Trojans a 45-42 come-from-behind victory.
Detroit selected Morton in the first round (21st overall pick) of the 1994 NFL Draft, and he played for the Lions from 1994 to 2001. He would go on to achieve an important secondary role on a deep Lions' receiving corps that also featured Pro Bowl flanker Herman Moore and veteran Brett Perriman. After learning the ropes as a rookie in 1994, Morton became Detroit's featured slot receiver in 1995 and a key contributor on special teams as a kickoff/punt returner. Morton was part of one of the most prolific offenses in Detroit history that year, as the Lions would rack up 436 total points (second highest in the NFL) and end up with ten victories - appearing in the playoffs for the third straight season. He contributed 44 receptions on that team for 590 yards and 8 touchdowns. Perhaps his most memorable game occurred that same season during a classic Thanksgiving Day game in Detroit against the Minnesota Vikings. Moore (127 yards), Perriman (153), and Johnnie Morton (102) all eclipsed the 100-yard receiving mark, and Hall of Fame running back Barry Sanders rushed for 138 yards, and quarterback Scott Mitchell passed for 410 yards in a 44-38 Lions' shootout victory.
After the departure of Perriman, Morton became more of a featured receiver in Detroit's offense in the ensuing years. His best season statistically was during the 1999 season when he had 80 receptions for 1129 yards on a surprising Lions team that made the playoffs that year, despite the unexpected retirement of Barry Sanders. All told, Morton finished his pro career with 624 receptions for 8719 yards and 43 touchdowns. He currently ranks third on Detroit's all-time list in both receptions and yards-receiving, with 469 and 6,499, respectively.
Morton had a brief cameo appearance in the movie Jerry Maguire and the television series Moesha.
During the 2001 season, comedian Jay Leno had been poking fun at the Lions' 0-12 record. When the Lions won their first game of the season 27-24 against the Minnesota Vikings, Morton, who knew of Leno's comments, said, "I got the damn monkey off my back, off Marty's back, and I want Jay Leno to kiss my ass." Morton later appeared on The Tonight Show, during which Leno kissed a donkey.