Drugovich made his single-seater debut in 2016 with Neuhauser Racing in ADAC Formula 4, achieving one podium at Zandvoort and finishing twelfth overall, fourth in the rookie standings. The following year he switched to Van Amersfoort Racing in ADAC Formula 4 and also debuted in Italian F4 with the team. He claimed seven wins in ADAC Formula 4 — the most of any driver in the season — and finished third in the standings with 236.5 points, nine points behind champion Jüri Vips, with a technical issue in the final round at Hockenheimring potentially costing him the title. He also competed in the MRF Challenge, winning the title the following year with ten wins from sixteen races.
Drugovich stepped up to the FIA Formula 3 European Championship with Van Amersfoort Racing for the 2017 season finale at Hockenheimring. He made his Euroformula Open debut as a guest with RP Motorsport at the final round of the 2017 season, taking a win. He then contested the full 2018 Euroformula Open season with RP, dominating the championship with a record fourteen wins and taking the title at Monza with two rounds to spare.
In 2019, Carlin confirmed Drugovich for the inaugural FIA Formula 3 Championship alongside Logan Sargeant and Teppei Natori. He scored points only once — sixth in race one in Hungary — and ended the season sixteenth with eight points.
Drugovich joined MP Motorsport for the 2020 Formula 2 season, partnering Nobuharu Matsushita. On debut in Austria, he qualified second and finished eighth before taking reverse pole and leading every lap in the sprint race for his maiden Formula 2 victory. He secured his first pole position at Silverstone, finishing seventh in the feature race and winning the sprint race by nine seconds. His campaign suffered a downturn at Spa-Francorchamps where contact with Matsushita caused a last-place finish compounded by a post-race disqualification for pitting on the final lap. He returned to form in Bahrain, winning the feature race by fourteen seconds after passing polesitter Callum Ilott on track. He concluded his rookie season ninth in the championship with 121 points, three wins, one pole, and four podiums.
Drugovich joined UNI-Virtuosi Racing for 2021 alongside Guanyu Zhou. He started strongly in Bahrain qualifying third but incidents and strategy issues compromised his results. In Monaco he secured his first podium of the season, finishing second in the first sprint race after inheriting the position following Christian Lundgaard's retirement. He endured a collision with Oscar Piastri in Baku's opening sprint, earning a ten-second penalty. He scored consistent points at Silverstone with finishes of fourth, sixth, and sixth. He crashed out at Monza and later at Sochi was declared unfit after crashing on the way to the grid. At the Abu Dhabi finale he finished second in the opening sprint and third in the feature race. He ended the season eighth in the standings with 105 points and four podiums.
Drugovich returned to MP Motorsport for 2022, partnering FIA Formula 3 graduate Clément Novalak. In Jeddah, Drugovich took his first pole of the season and dominated the feature race to take the championship lead. In Barcelona, despite a three-place qualifying penalty for impeding, he won both the sprint and feature races — the first driver to win both races of a Formula 2 weekend. In Monaco, he inherited pole following a penalty for Liam Lawson and won the feature race despite a puncture in the sprint. He secured consecutive poles at Zandvoort and won the feature race, extending his championship lead to 69 points. At Monza, contact with Amaury Cordeel ended his sprint race early, but Théo Pourchaire's non-scoring finish confirmed Drugovich as the 2022 FIA Formula 2 Champion. He closed the season with 265 points, 101 ahead of Pourchaire, recording five wins, four poles, and eleven podiums.
On 12 September 2022, two days after clinching the Formula 2 title, Drugovich was announced as the first member of the newly formed AMF1 Driver Development Programme and joined Aston Martin as a reserve driver. He tested the AMR21 at Silverstone in November 2022 and participated in free practice at the 2022 Abu Dhabi Grand Prix. For 2023, alongside fellow Aston Martin reserve Stoffel Vandoorne, he was added to McLaren's reserve pool for the first 15 races. He drove the AMR23 during pre-season testing in Bahrain after Lance Stroll sustained an injury in a cycling accident, completing 117 combined laps over the test. He also made free practice appearances at the Italian Grand Prix and Abu Dhabi Grand Prix that year.
In 2024, Drugovich continued as Aston Martin's test and reserve driver, making free practice appearances at Mexico City (18th fastest) and Abu Dhabi (9th fastest). In 2025, he made a free practice appearance at the Bahrain Grand Prix, finishing sixteenth — less than a tenth behind Lance Stroll — and stepped in for Fernando Alonso during first practice at the Hungarian Grand Prix after the Spaniard sustained an injury. He departed Aston Martin following the Las Vegas Grand Prix after signing with Andretti for Formula E.
In April 2023, Drugovich was selected to drive for Maserati MSG Racing in the Formula E Berlin rookie test, finishing first with a lap only two tenths slower than the fastest time in the SABIC Berlin E-Prix set by Maximilian Günther. He returned with Maserati for the Rome ePrix rookie session, again topping the timesheets, and for the 2024 Berlin rookie test.
Drugovich made his Formula E race debut at the 2025 Berlin ePrix with Mahindra Racing alongside Edoardo Mortara, replacing an absent Nyck de Vries. A drive-through penalty due to a gearbox change ruined his first race (17th), but in the second race two late Attack Mode activations allowed him to climb to seventh and score his maiden Formula E points.
Andretti subsequently signed Drugovich for the full 2025–26 Formula E season alongside 2022–23 champion Jake Dennis. At the season opener in São Paulo, a penalty for overtaking under a full-course yellow dropped him from fifth to 12th. In Mexico City he finished 15th. He qualified second for the Miami ePrix but misjudged his braking point on lap 26, hitting António Félix da Costa's Jaguar; a pit stop for a new front wing and a ten-second penalty resulted in 18th place. At Jeddah he finished 15th and 12th across two races.
Drugovich returned to endurance racing in the 2024 European Le Mans Series with Vector Sport, partnering Stéphane Richelmi and Ryan Cullen. The trio finished tenth in class in the opening two races, then third at Imola after a successful pit strategy. Drugovich also competed in his first 24 Hours of Le Mans in 2024 with Whelen Cadillac Racing, finishing 15th in the Hypercar class. For 2025, he signed with Cadillac Whelen Racing for the 24 Hours of Daytona. Drugovich was offered the opportunity to test for IndyCar team Ed Carpenter Racing but declined; he later tested IndyCar machinery with Chip Ganassi Racing at Barber Motorsports Park, describing himself as "surprised by the speed".
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