On 29 June 2007 he officially joined Milan's academy, where he spent the following ten years, playing through the different age groups up to the Primavera (under-19) team.

[12][13] In the summer of 2017, Cutrone signed a contract extension until 30 June 2021,[14] while Milan's Chinese-led board of directors spent over €200 million on transfers, acquiring a total of 11 new players, two of which were strikers André Silva and Nikola Kalinić.

[20] Coming on as a substitute in the Coppa Italia match against local rivals, Internazionale, Cutrone scored the winner and his first goal in the Derby della Madonnina.

[22] Although it was reported that Cutrone may possibly get a two-match ban for an alleged deliberate handball,[23] an investigation conducted by governing body the FIGC proved that his actions in that episode were unintentional and, therefore, non-punishable.

[25] In the summer of 2018, Milan's new board of directors decided to increase the team's attacking capability with the signing of a high-profile goalscorer, Gonzalo Higuaín, whom Cutrone first met in 2015 as a fan.

[28][29] On 31 August 2018, Cutrone came on as a late substitute and scored a last-minute match-winning goal in a 2018–19 Serie A home game against Roma (2–1), helping Milan secure the very first competitive victory in the season.

[32] In the same month, the club opted for an early termination of Gonzalo Higuaín's loan and bought Krzysztof Piątek as a first-choice striker, whose role on the pitch and style of play were considered "too similar" with those of Cutrone.

[33] The team's head coach, Gennaro Gattuso, also refused to pair strikers for tactical reasons and preferred 4–3–3 as his regular starting formation.

[34] As a result, Cutrone's playing time and quality of performances continued to decrease, with the player failing to score or assist in his 18 consecutive appearances, mostly as a super-sub.

[35][36] Despite Giampaolo favoring 4–3–1–2 over any other formation, Cutrone's opportunities at Milan were still considered limited as the new coach sought to pair Piątek with a different type of an attacking partner than him.

[41] On 15 August, Cutrone made his full debut for Wolves in a 4–0 home win against FC Pyunik in the 2nd Leg of the UEFA Europa League Third Qualifying Round.

[69] Apart from his regular position as a central striker,[70] Cutrone has also been used as a makeshift left winger by his former Milan coach Gennaro Gattuso, in a role similar to that of Mario Mandžukić at Juventus.

[72] Former Milan forward Daniele Massaro likened Cutrone to himself in 2019, also referring to the latter as a "supersub," due to his penchant for scoring decisive goals after coming off the bench.

[73] In 2021, Cutrone visited the UEFA Euro 2020 Final played in London at Wembley Stadium between Italy and England, cheering his compatriots to victory amongst the crowd of about seven thousand Italian supporters.