James Stewart entered the league as a foundational piece for the expansion franchise when he was taken 19th overall from Tennessee. A physical, between-the-tackles runner listed at 6-foot-1 and 224 pounds, he carried a heavy operational load during the club's inaugural campaign, leading the backfield with 525 rushing yards and scoring the first rushing touchdown in team history.

Stewart played an integral role in Jacksonville’s rapid ascent to contention, operating as a reliable short-yardage finisher and dual-threat option. During the 1996 Cinderella postseason run to the AFC Championship Game, his inside running provided crucial balance alongside Mark Brunell's scramble drills. In an October 1997 matchup against Philadelphia, Stewart etched his name into team record books by rushing for five touchdowns in a single game—a franchise record that still stands.

Despite sharing backfield touches after Fred Taylor arrived in 1998, Stewart remained a critical red-zone weapon. His final year with the organization in 1999 yielded his most efficient production, as he amassed 931 rushing yards and crossed the goal line 13 times on the ground for a 14–2 squad that reached another AFC title game.

Entering free agency after five seasons, Stewart signed with the Detroit Lions in 2000 and produced two 1,000-yard campaigns before injuries forced his retirement after the 2002 season.  In Jacksonville, Stewart had 65 carries for 2,951 rushing yards, 33 rushing touchdowns, 101 receptions for 828 receiving yards, and five receiving touchdowns.