Established as the Durham Tobacconists in the North Carolina League in 1902, the team subsequently disbanded and restarted numerous times.

Though not affiliated with any MLB team for the first four, the Bulls were a farm club for the Cincinnati Reds and Brooklyn Dodgers, respectively, for the last two.

They won the Carolina League championship on three occasions: in 1957 with the Detroit Tigers, 1967 with the New York Mets, and 1969 with the Philadelphia Phillies.

The Bulls have won the International League championship eight times (2002, 2003, 2009, 2013, 2017, 2018, 2021, and 2022), all as an affiliate of the Tampa Bay Rays.

On May 30, 1917, however, the North Carolina State League folded due to America's joining of the Allied Powers during World War I.

The park was dedicated on July 26 by the Commissioner of Baseball Kenesaw Mountain Landis, who put on a show by riding a real bull, the team mascot, onto the playing field.

On the evening of June 17, 1939, the Durham Athletic Park burned to the ground hours after the Bulls defeated the Portsmouth Cubs 7-3.

The groundskeeper, Walter Williams, who was asleep under the grandstand when the blaze began, was able to escape though the fire nearly killed him.

In a remarkable two-week turnaround, Durham Athletic Park was functioning again by July 2, with the old wooden grandstand replaced by concrete and steel.

Three years later, in September 1948, Tom Wright, a former Bulls outfielder, became the first Carolina League player to make it to the majors when he debuted with the Boston Red Sox.

When the film Bull Durham was released in mid-1988, it led to a major resurgence of local popular interest in the team and their ballpark.

On August 30, 1990, a crowd of 6,202 made the Bulls the first Class-A team in history to pass the 300,000 mark in attendance for a season.

Capitol president Jim Goodmon initially proposed building the new stadium near Raleigh-Durham International Airport, but after city leaders in Durham offered to renovate the old ballpark or help build a new stadium, the current downtown Durham site was secured.

The 1997 season was the final one in which the Bulls were an affiliate of the Atlanta Braves and also their last year in the High-A Carolina League.

The real Jim Morris did play for the Bulls briefly during the 1999 season and was then called up to the major leagues on September 18, 1999, at the age of 35.

In 2003, Durham became the first club in the 119-year history of the championship to sweep back-to-back final playoff series, defeating the Pawtucket Red Sox.

The third time was the charm for the Bulls in the Governors' Cup final, as they dethroned the Scranton/Wilkes-Barre Yankees in three games to win the championship, their third since joining the International League.

On August 2, 2011, the Bulls defeated the Charlotte Knights, the Chicago White Sox affiliate, 18-3 for their 6,000th win in franchise history.

In 2013, the team won its fourth Governors' Cup title, defeating the Pawtucket Red Sox in the International League Final.

On August 31, 2014, the Bulls again broke their all-time paid attendance record, finishing the year with a cumulative mark of 533,033.

Before the 2015 season, Jared Sandberg was named the fourth manager in the team's Triple-A history, replacing Montoyo.

The Bulls then won their second Triple-A National Championship, defeating the Memphis Redbirds after beating the Scranton/Wilkes-Barre RailRiders for their fifth Governors' Cup title.

[12] The team finished 2019 with a 75-64 record, making the playoffs as a wild card, and advanced to the Governor's Cup before losing to Columbus.

[13] As a consequence of the worldwide onset of the COVID-19 pandemic, Minor League Baseball announced on June 30, 2020, that no season would be held, meaning that the Durham Bulls would not take the field again until the following spring.

[20] They then defeated the Nashville Sounds, winners of the Western Division, in a single playoff game, 13–0, to win the IL championship.

[22] Playing under a split-season format in 2023 in which the teams with the best league-wide records at the end of each half qualified for the playoffs,[23] Durham won the second-half title at 48–27.

[25] In a single round of playoffs for the IL championship versus the Norfolk Tides, winners of the first-half, the Bulls were defeated, two games to one.

[152] All home and road games can be viewed through the MiLB.TV subscription feature of the official website of Minor League Baseball, with audio provided by a radio simulcast.

[153] Former play-by-play announcers include Gary Cohen, who was the Voice of the Bulls in 1986 and became part of the New York Mets' broadcast team in 1989,[154] Steve Barnes (who also was the Duke women's basketball radio play-by-play announcer),[155] and Neil Solondz, who was with Durham from 2004 to 2011 before being hired by the Tampa Bay Rays.

[157] Broadcasts are produced by members of Explorer Post 50, a youth-based group for students who have completed middle school and are 14 to 20 years old.