The university first fielded a football team in 1972, and the Dukes play at the on-campus Bridgeforth Stadium in Harrisonburg, Virginia.

The Dukes won their second national championship in 2016 and finished as national runners-up in 2017 and 2019. Notable Dukes include Charles Haley, one of two players to win five Super Bowl rings and is also an inductee of the College Football Hall of Fame and Pro Football Hall of Fame;[2] Scott Norwood, of the Buffalo Bills; Gary Clark, an All-Pro wide receiver for the Washington Commanders; Arthur Moats, a linebacker for the Buffalo Bills and Pittsburgh Steelers who is known for delivering the sack that led to the end of the record streak of consecutive starts made by Brett Favre in the National Football League (NFL); and Aaron Stinnie, an offensive guard for the New York Giants who won a Super Bowl with the 2021 Tampa Bay Buccaneers.

Football was the brainchild of Dr. Ronald Carrier, Madison's president at the time, who was attempting to change the psychology of the campus away from an all-women's teachers college.

[3] The first game took place on October 7, 1972, against Shepherd College's junior varsity team at Harrisonburg High School.

In the second week of the 2010 season, JMU beat then #13 FBS ranked Virginia Tech in Blacksburg 21-16[6] A $62 million stadium expansion to Bridgeforth was completed in 2011, adding an upper deck, club seating and 17 private suites.

[9] Prior to his work at Ohio State, Withers was interim head coach for North Carolina during the 2011 season after the dismissal of Butch Davis.

[10] His first win as interim head coach at North Carolina was against the Mickey Matthews led James Madison Dukes on September 3, 2011.

He also helped JMU receive national attention when ESPN's College GameDay show traveled to Harrisonburg to feature the 2015 Dukes.

On January 18, 2016, James Madison named Mike Houston as head coach of the Dukes football program.

JMU won the National Championship in decisive fashion, with a score of 28–14 (Youngstown State scored a meaningless touchdown with seconds left in the game) on a cold, 15 °F afternoon in Frisco, Texas On January 7, 2017, JMU faced the Youngstown State Penguins for the 2016 FCS National Championship at Toyota Stadium in Frisco, Texas.

[18] After a first-round bye, JMU faced the Stony Brook Seawolves in the FCS Second Round, winning by a score of 26-7.

Trailing late in the 4th quarter, JMU eventually won the game on a last second field goal, advancing to the FCS semifinals to face South Dakota State, from the Missouri Valley Football Conference.

In this game, the Dukes, bolstered by 10 takeaways on defense, cruised to an easy 51-16 victory,[20] and earned a return trip to Frisco, TX to defend their 2016 National Championship.

In the Title game, the Dukes were plagued by dropped passes and uncharacteristic turnovers, and fell to the North Dakota State Bison by a score of 17-13.

[34] #2 James Madison came three yards shy of forcing a potential overtime in the NCAA Division I Championship Game, but a late interception sealed a third consecutive national title for #1 North Dakota State in a 28-20 victory for the Bison on Saturday afternoon at Toyota Stadium.

JMU's 2019 senior class finished their careers with the most wins in school history, with 51 victories,[36] and the Dukes are now 2-2 overall in national-title games.

[38] Subsequently, James Madison announced they had finalized their departure from the CAA on February 2, 2022, and would join the FBS and the Sun Belt for the 2022-23 season.

[39] JMU's arrival in FBS made the Dukes the second program, after UCF, to have played at all four current levels of NCAA football.

On October 26, 2022, the JMU Dukes and in-state rival Old Dominion Monarchs announced the official beginning of the "Royal Rivalry".