Rossi established the team in 2014 in response to what he perceived as an overwhelming influx of Spanish riders into Grand Prix racing. The objective was to identify and develop promising Italian riders, with Rossi's former Cagiva teammate Vittoriano Guareschi serving as the initial team manager. Pablo Nieto later took over management duties and has continued in the role.
The team entered Moto3 as Sky Racing Team VR46, choosing Romano Fenati and Francesco Bagnaia as its first riders. Fenati scored four wins in the debut season. Subsequent Moto3 seasons saw the team develop multiple riders, including Andrea Migno, Nicolò Bulega, Celestino Vietti, and Dennis Foggia. Vietti was a consistent performer in the latter seasons, helping the team to third place in the teams' championship in 2020. VR46 stepped away from Moto3 after 2020, citing a shortage of available Italian talent relative to the number of Italian-aligned junior teams.
VR46 entered Moto2 in 2017 with Bagnaia and Stefano Manzi. Bagnaia's arrival in the class was immediate and dominant: he finished second in his fourth-ever Moto2 race at Jerez and collected multiple wins before clinching the 2018 Moto2 World Championship, the team's only riders' title to date. That season Luca Marini, Rossi's half-brother, joined as second rider and finished seventh in the standings.
In 2020, Marco Bezzecchi partnered Marini, and the team produced an exceptional Moto2 campaign. Between them, Marini and Bezzecchi won five races, and VR46 claimed the Moto2 Teams' Championship — their first teams' title. Marini finished second in the riders' standings and Bezzecchi fourth. Following the 2022 season, the VR46 Moto2 entry was absorbed into a Fantic-branded programme.
In 2021, Marini made his MotoGP debut via an arrangement with Esponsorama Racing, with the bike operating under VR46 colours. Beginning in 2022, VR46 took full ownership of its MotoGP presence, fielding Marini and Bezzecchi with Ducati Desmosedici machinery under a factory-support agreement with Ducati Corse.
The 2023 season saw Bezzecchi mount a genuine championship challenge, winning in Argentina, France, and India. The team operated with the Ducati Desmosedici GP22 that year, one generation behind the factory bikes, yet Bezzecchi remained in contention until late-season injuries disrupted his campaign.
For 2024, Luca Marini departed to join the Repsol Honda factory team, with Fabio Di Giannantonio taking his place alongside Bezzecchi. From 2025, Ducati upgraded VR46's status to factory-backed, providing the team with current-specification machinery. Bezzecchi left for Aprilia after 2024 and was replaced by Franco Morbidelli, who joined from Pramac Racing.
The VR46 Racing Team has accumulated 32 race victories across its three active class programmes: nine in Moto3, nineteen in Moto2, and four in MotoGP. Its championship titles include the 2018 Moto2 riders' title with Bagnaia and the 2020 Moto2 teams' title.
The team's association with Valentino Rossi extends beyond ownership; it embodies the ethos of a specific Italian motorsport culture centred on Rossi's home region. The team's base in Tavullia, Rossi's hometown, and its deliberate focus on Italian development riders reflects a vision that distinguishes it from the commercially-driven satellite team model prevalent in MotoGP.