Ashcroft was nominated as a
father–son selection for the
Brisbane Lions in the
2022 AFL draft, and was accepted as Pick 2 after the Brisbane Lions matched
North Melbourne's bid. He since agreed to remain with the Brisbane Lions until at least the end of the 2026 season. Ashcroft made his AFL debut in Round 1 against
Port Adelaide, gathering 13 disposals and a goal in a 54-point defeat. In Round 2, Ashcroft collected 31 disposals against
Melbourne and received a
Rising Star nomination as one of the best players on the ground in only his second game, earning widespread praise from the AFL media and community. In Round 19, Ashcroft ruptured his ACL against the
Geelong Cats, ending his debut season prematurely and therefore missing the 2023 finals series. The AFL community all widely expressed their support for Ashcroft, who was the Rising Star favourite and had been a standout player for Brisbane despite it being his debut season. He documented his recovery process through his website, WASH Performance and Wellbeing. Ashcroft's was nominated for and won the
Goal of the Year, announced at the
2023 Brownlow Medal. He finished the year with 10 Brownlow votes, the third-most for the Lions, finishing behind
Joe Daniher with 12, and
Lachie Neale, who won the award with 31. He was also selected in the 2023
22under22 team. He returned from his ACL injury mid-way through the 2024 season, returning against Melbourne in Round 16 and playing a crucial role in the Lions' mid-season resurgence that saw them bounce back from a below-average season start to make finals with a fifth-place finish. Ashcroft would be instrumental in the Lions finals run, and was part of the Brisbane Lions
2024 premiership winning team, winning the
Norm Smith Medal as best afield in the Grand Final with 30 disposals and a goal. At 20 years of age, Ashcroft became the youngest Norm Smith Medal winner since 1979, when
Wayne Harmes won the inaugural edition of the award. He also became the first Queenslander to win the Norm Smith Medal in 2024. On 4 May 2025, Brisbane defeated the Gold Coast Suns in
QClash 28, winning 9.12 (66) to 7.7 (49). Ashcroft accumulated 34 disposals, 17 contested possessions and 9 clearances to be awarded the
Marcus Ashcroft Medal as the best on ground. The medal is named after his father, due to his contributions to both clubs. On 19 August, Ashcroft received his second
22under22 selection, being selected in the 2025 team. For the second year running, Ashcroft was key to the Lions' finals run, winning a second premiership in a row in the
2025 Grand Final, this time enjoying premiership success alongside his brother
Levi. Ashcroft won the Norm Smith Medal for the second year in a row, becoming one of only five players to win the medal multiple times and one of only three players to win it two years in a row. He is the youngest dual Norm Smith medallist in VFL/AFL history. Ashcroft also won the 2025
Gary Ayres Award, awarded to the best player across the finals series. In December 2025, the AFL confirmed Ashcroft's
State of Origin eligbility would be tied to Queensland after missing out on selection for the
2026 AFL Origin match. ==Statistics==