Bonaventura started his senior career at Atalanta in the Serie A in 2007; his impressive performances earned him a €7 million transfer to AC Milan in 2014, where he spent six seasons.

After playing for San Francesco 93' youth team, he was transferred to Tolentino, where he was noticed by one of Atalanta's scouts, Antonio Bongiorni.

In June 2010, Padova decided not to buy him outright,[5] and Bonaventura returned to Atalanta, signing a contract extension until 2015.

[7] In late August, Atalanta and Hellas Verona had agreed for the signature of Bonaventura and Verona's ex sporting director, Sogliano, had talked to Giacomo but on 1 September 2014, in the last hours of the Italian transfer window, AC Milan announced the signature of Bonaventura from Atalanta for a fee reported to be around €7 million after they failed to sign Jonathan Biabiany.

[16] On 19 September, Bonaventura assisted Carlos Bacca's first goal and scored directly from a free-kick in a 3–2 win over Palermo.

[18] He ended the season with 7 goals and 8 assists in all competitions as Milan finished 7th in Serie A, and lost out in the Coppa Italia final against Juventus, following a 1–0 defeat in extra time.

[24] On 23 December 2016, Bonaventura scored the equalising goal in the Supercoppa Italiana against Juventus; he later netted his penalty in the resulting shoot-out, helping Milan to a 4–3 victory.

[28] He returned to the squad for the last game of the season against Cagliari on 28 May, but couldn't make an appearance during the match as Milan lost 2–1.

[29][30] He ended the season with 5 goals and 4 assists in 22 appearances in all competition as Milan finished 6th in Serie A, was knocked out of Coppa Italia in quarter-finals by eventual champions Juventus, and also won the Supercoppa Italiana.

Bonaventura played his first game in Europe in a 1–0 win against CS U Craiova in the first leg of Milan's Europa League qualification match on 27 July 2017.

His last appearance for the club was as a substitute in a 3–0 win against Cagliari at the final day of the season, coming on for Rafael Leão in the 38th minute.

[45] On 5 August 2024, Saudi Pro League club Al-Shabab signed Bonaventura on a one-year contract, with an option for a second year.

[46] After featuring with under-19, under-20 levels, Bonaventura made his debut with the senior squad on 31 May 2013, in a 4–0 friendly victory against San Marino in Bologna, under Cesare Prandelli.

[47] His second appearance for Italy came 16 months later, in a friendly against Albania, during which he managed to assist Stefano Okaka's match–winning goal in a 1–0 victory in Genoa.

[50] At 34 years, one month and 22 days, Bonaventura became the oldest player to score his debut goal for Italy when he found the back of the net against Malta in a Euro 2024 qualifier at Stadio San Nicola in Bari on 14 October 2023.

He has also been deployed in a box-to-box role on occasion, a position in which he was described as a tuttocampista, in the Italian media, namely a player who covers the entire pitch.

He is talented in keeping possession effectively, due to his ball skills and dribbling ability, and also excels at creating space or chances for teammates through his movement and awareness.