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Club formation and play in the USL first division

On January 26, 2006, the expansion of the USL to Cary, North Carolina, was announced at a press conference at SAS Soccer Park, since renamed WakeMed Soccer Park. After a few changes in the 2008 off-season, the RailHawks ownership group consisted of Wellman Family Limited partnership (Selby and Brian Wellman), HTCFC. INC (Bob Young former CEO of Red Hat, presently founder and CEO of LULU.com), Singh Holdings (Dr. H. Paul Singh) and Boris Jerkunica. After the 2010 season, Traffic Sports USA took ownership.

On October 11, 2006, former Rochester Rhinos defender Scott Schweitzer was named the first head coach of the RailHawks. Schweitzer played collegiately at North Carolina State University and retired from play prior to the 2006 season. On December 5, 2006, the RailHawks named the first players to sign with the franchise. Among the signings were two former UNC Tar Heel players, Chris Carrieri and Caleb Norkus, as well as several other players with Major League Soccer, United Soccer Leagues, and foreign playing experience.

The club launched their inaugural season on April 21, 2007, in front of a crowd of 6,327 at SAS Soccer Park when they drew 1–1 with the Minnesota Thunder in their first official regular season match. Midfielder Kupono Low scored the first goal in franchise history when he blasted a 24-yard left-footed shot past Thunder keeper Joe Warren in the 8th minute of the inaugural match. On May 8, 2007, the RailHawks earned their first franchise victory 2–0 against Chivas USA in an exhibition match.

On August 14, 2007, with a 3–0 victory over the Charleston Battery, the RailHawks secured their first piece of silverware, the 2007 Southern Derby Cup, with one match remaining in the contest. The RailHawks finished their first USL-1 season in 8th place in the league table, securing the league's final playoff spot on the last day of the regular season with a 2–0 victory away over fellow expansion franchise the California Victory. The RailHawks were eliminated from the playoff quarterfinals by the eventual league champion Seattle Sounders.

Move to the NASL

In November 2009 the RailHawks announced their intent to leave the USL First Division to become the co-founders of a new North American Soccer League, which would begin play in 2010. The league, which had yet to be sanctioned by the United States Soccer Federation or the Canadian Soccer Association, also comprised the Atlanta Silverbacks, Crystal Palace Baltimore, Miami FC, Minnesota Thunder, Montreal Impact, Tampa Bay Rowdies, Vancouver Whitecaps and a brand new team led by St. Louis Soccer United.

After lawsuits were filed and heated press statements exchanged, the USSF declared they would sanction neither league for the coming year, and ordered both to work together on a plan to temporarily allow their teams to play a 2010 season. The interim solution was announced on January 7, 2010, with the USSF running the new USSF D-2 league comprising clubs from both USL-1 and NASL. The RailHawks reached the final of the USSF D-2 playoffs, but fell to the Puerto Rico Islanders. After the 2010 season, the NASL and USL split, but the RailHawks faced sale by Selby Wellman on December 31, 2010. The RailHawks name was sold on eBay and was purchased by Traffic Sports USA, who assumed operations of the club. The NASL received provisional sanctioning in 2011 and full sanctioning in 2012.

The RailHawks won the regular season in 2011 but fell to the NSC Minnesota Stars in the semifinals of playoffs. The club hired Colin Clarke as coach after Martin Rennie left for the Vancouver Whitecaps. In 2012, the RailHawks finished 4th in the regular season and fell to the Tampa Bay Rowdies in the playoff semifinals, while reaching the fourth round of the US Open Cup.

In 2013 the NASL's format changed to a split season, and though the RailHawks finished with the most points in the league, they finished 2nd in both the Spring and Fall seasons and did not make the Soccer Bowl. However, they defeated MLS teams LA Galaxy and Chivas USA to advance to the quarterfinals of the US Open Cup. In 2014, the RailHawks again defeated Chivas USA and Los Angeles Galaxy to reach quarterfinals of the US Open Cup, but fell just short of reaching the NASL playoffs.

In 2015, the club saw a change in ownership as local businessman Steve Malik took over the team from Traffic Sports. During a press conference on October 30, 2015, the ambitious local owner said, “Our goal is to take the RailHawks to the highest level through additional investment in marketing, players and staffing. We are excited to lead our community in working together to give the Triangle a world-class soccer team.”

New faces in the front office were matched with the new faces on the field. The RailHawks had a big year in 2016 with the addition of forwards Omar Bravo and Matt Fondy. Bravo, the biggest signing in club history, provided senior leadership and immense experience to the team, as he left C.D. Guadalajara as the team's all-time leading scorer. Though the RailHawks missed the playoffs again, with a 7W-5D-10L record, they again made an impressive Open Cup run, reaching the fourth round where they lost a tight 1–0 game to the New England Revolution of MLS. In the third round, the RailHawks eliminated the Charlotte Independence with a 5–0 win that saw Carolina score five extra-time goals in the thrilling match. The score set a US Open Cup record for the most goals scored by a single team in extra time.

Also in 2016, West Ham United became the first Premier League team to visit the Triangle region of North Carolina when they came to WakeMed Soccer Park on July 12, 2016. The game ended in a 2–2 draw in front of a record-breaking crowd of 10,125.

Return to the USL

On November 16, 2017, the club announced it would be leaving the NASL to join the USL for the 2018 season. The club announced, on October 17, 2018, that head coach Colin Clarke would not be returning to the club after seven seasons and that the club has begun searching for a new head coach.

Dave Sarachan, the former U.S. Men's National Team coach, was named as the fourth head coach in club history on December 17, 2018. They clinched a spot in the USL Championship Playoffs on September 30, 2019.

Drop to USL League One

On January 10, 2021, club chairman Steve Malik announced that the club would make a "strategic move" to USL League One, the third-division of the United States soccer league system. Along with the move to USL League One, coach Dave Sarachan and North Carolina parted ways. In their final season in USL League One, North Carolina FC defeated rivals Charlotte Independence on penalties 1-1 (5-4) to win the 2023 USL League One Finals, securing their first title in franchise history.

Return to USL Championship

On August 7, 2023, the club announced they were exercising their option to rejoin the USL Championship beginning in the 2024 season.