Rossi founded the team in 2014 with the explicit purpose of promoting young Italian talent in Grand Prix racing, motivated by the large influx of Spanish riders that had dominated the junior classes since the early 2000s. The team entered the Moto3 World Championship as Sky Racing Team VR46, fielding Romano Fenati and Francesco Bagnaia in its opening year, with Rossi's former Cagiva teammate Vittoriano Guareschi as team manager.
Fenati took four victories in the debut season. Pablo Nieto subsequently replaced Guareschi as team manager. The Moto3 programme developed further talents including Andrea Migno, Nicolò Bulega, Celestino Vietti, and Dennis Foggia before the team exited Moto3 after 2020, citing a lack of available Italian talent relative to the number of Italian Moto3 teams competing at the time.
In 2017 the team expanded into Moto2, selecting Bagnaia and Stefano Manzi as its riders. Bagnaia was immediately competitive, claiming multiple podiums in his debut Moto2 season and finishing fifth in the championship. For 2018, Bagnaia was joined by Luca Marini — Valentino Rossi's half-brother — and delivered one of the strongest Moto2 seasons seen from the team. Bagnaia won eight races, dominated the second half of the season, and was crowned Moto2 World Champion. Marini also took a victory in Malaysia, with the pair finishing the teams' championship in second place.
In 2020, Marini was partnered with Marco Bezzecchi. Both riders performed strongly, Marini taking three wins and six podiums and Bezzecchi adding two wins and seven podiums. VR46 clinched the Moto2 teams' championship — their first — with Marini and Bezzecchi placing second and fourth respectively in the riders' standings.
VR46 entered MotoGP proper in 2022, taking over the grid slots from Esponsorama Racing, which had hosted Luca Marini under the VR46 banner in 2021. The team debuted with Marini and Bezzecchi on Ducati Desmosedici machinery under a partnership with Ducati Corse signed in June 2021.
In 2023, Bezzecchi mounted a serious championship challenge, winning in Argentina, France, and India and running near the front of the standings before injuries and the limitations of running a year-old machine derailed his campaign. The team announced Indonesian lubricant brand Pertamina as title sponsor from 2024.
For 2024, Marini departed to join Repsol Honda and was replaced by Fabio Di Giannantonio. The team maintained its Ducati partnership and received factory-backed support from 2025, with Di Giannantonio fielding an official Desmosedici.
Bezzecchi left VR46 after 2024 to join Aprilia, and Franco Morbidelli joined from Pramac Racing for 2025.
The VR46 Racing Team embodies Rossi's vision of a talent factory for Italian Grand Prix racing, having launched the careers of Bagnaia — who went on to win back-to-back MotoGP titles with Ducati in 2022 and 2023 — as well as a generation of Italian riders who progressed through its Moto3 and Moto2 programmes. The team's trajectory from Moto3 newcomer to MotoGP factory-backed outfit within a decade reflects both Rossi's influence in the paddock and Ducati's investment in building an ecosystem of competitive satellite teams.