North Dakota won the NCAA Division II national championship in 2001, defeating Grand Valley State 17-14 in Florence, Alabama, with quarterback Kelby Klosterman throwing 32 touchdowns and running back Jed Perkerewicz scoring the game-winning touchdown with 29 seconds left. That championship remains the program's highest achievement and the anchor of its identity.

The Hawks joined Division I FCS in 2008 and transitioned from the "Fighting Sioux" name to "Fighting Hawks" between 2015-2016, following NCAA policy on Native American team names. The change came after the Standing Rock Sioux tribe did not approve retaining the old name, while the Spirit Lake tribe approved it. When the school's Board of Higher Education voted to retire the name in 2012, the Hawks were chosen in 2015 with 57.24% of the vote.

North Dakota joined the Missouri Valley Football Conference in 2020, reuniting historic Division II rivals (NDSU, South Dakota, South Dakota State) at the FCS level for the first time in 16 years. In 2025, under first-year head coach Eric Schmidt—who played for the 2001 championship team and was its captain—the Hawks finished 7-5 and made the FCS playoffs, defeating Tennessee Tech 31-6 before losing to Tarleton State 31-13. The season's defining moment came on November 8, when North Dakota State clinched the MVFC title 15-10 over UND in what may be their final annual meeting. NDSU announced its move to the Mountain West Conference and FBS in February 2026, marking the second time realignment has interrupted the historic rivalry—first when the Nickel Trophy was retired after 2003, and now as NDSU departs for a higher level.