According to sports historian Peter Stewart, in September 1930 a reporter asked Coach Tommy Scott whether the Norfolk Division of the College of William & Mary should have a football team.

Scott answered that he had not thought of having one, but within two days a team was "put together hurriedly" and began playing other small colleges.

The team lost every game in its last season, attendance was small, and Stewart believes that World War II would likely have forced the program to end regardless of other reasons.

[5] According to Senior Associate Athletic Director Debbie White, ODU had tried several times to restart a football team.

The university wanted to improve ties to alumni, who often stated in exit interviews before graduation their wish for an ODU football team, and rarely revisited the campus.

Old Dominion began play in 2009 as an independent team at the Division I FCS level (formerly I-AA), and joined the Colonial Athletic Association (CAA) for the 2011 season.

Wilder's inaugural team finished the year ranked in the top ten in five FCS statistical categories, including second in sacks allowed, third in scoring offense, turnover margin and net punting.

In its first three years of competition after its rebirth, Old Dominion compiled a 26–7 record and earned a berth in the 2011 FCS playoffs, hosting and defeating its crosstown rival Norfolk State.

Also in 2011, after playing 27 games in its "modern era", ODU received its first Top 25 ranking on October 3, coming in at No.

On 26 November 2011 the ODU Monarchs beat their crosstown rivals, the Norfolk State Spartans, 35–18 to advance to the second round of the 2011 FCS playoffs.

By finishing the regular season 10–1, the Monarchs won an at large bid into the 2012 NCAA Division I FCS Playoffs.

[17] ODU began its transition to the NCAA Division I Football Bowl Subdivision (FBS) at the conclusion of the 2012 season.

Originally, the 2014 season was to be spent as an FBS independent before being fully accepted into the C-USA with both bowl and championship eligibility.

[25] Ricky Rahne, former Penn State offensive coordinator, was announced as the next head coach on December 10, 2019.

[26] Amid the COVID-19 pandemic, the university announced that the 2020 football season for the Monarchs was canceled due to concerns about the safety of athletes and coaches.

After a 1-5 start ODU went on a 5 game winning streak to end the regular season 6-6; while becoming Bowl eligible for the second time in program history.

As the Monarchs across all sports moved into the Sun Belt Conference in July of that year, leaving C-USA (along with Southern Miss and Marshall).

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

A declared rivalry with the William & Mary Tribe lasted two years before the Monarchs began their FBS transfer process in 2013.

[31] Despite ODU's transfer to the FBS, Norfolk State remained on the Monarchs' schedule as an FCS opponent for their 2015 and 2019 seasons.