[5] At the end of the season Bernareschi scored 12 goals in 39 appearances and Crotone exercised the option to acquire half the player's contract in co-ownership.

[6] On 20 June 2014, Fiorentina officially redeemed Crotone's half of Bernardeschi's contract,[7] and he was inserted into the first team under the direction of Vincenzo Montella.

[11] He was awarded the number 10 shirt at the start of the 2015–16 season, previously worn by the likes of Giancarlo Antognoni and Roberto Baggio.

[18] He made his UEFA Champions League debut on 12 September, coming on as a second-half substitute for Rodrigo Bentancur in a 3–0 away loss to Barcelona.

[23] On 9 February 2018, Bernardeschi returned to Florence, receiving vulgar insults from home fans throughout the match; he scored a free kick in the second half to silence the crowd.

[24] Bernardeschi scored his first goal of the 2018–19 season in Juventus's opening Serie A match on 18 August 2018, netting the winner in a 3–2 away victory over Chievo in injury time.

[25] On 12 March 2019, Bernardeschi made a great sprint that resulted in a penalty kick in a 3–0 win over Atlético Madrid in the Champions League.

[27][28] On 26 July, he scored his first and only league goal of the season in a 2–0 home win over Sampdoria, which allowed Juventus to clinch the Serie A title.

[29] During the second-half of the 2020–21 season under new manager Andrea Pirlo, Bernardeschi was converted into a full-back for Juventus after excelling in the position in a Coppa Italia win against Genoa on 13 January 2021.

[30] On 15 July 2022, Bernardeschi signed for Major League Soccer club Toronto FC as a designated player on a four-year contract; he reunited with Italian compatriots Lorenzo Insigne and Domenico Criscito.

[33] In the 2022 Canadian Championship Final against Vancouver three days later at BC Place, he set-up Lukas MacNaughton's temporary equaliser in the second half with a trivela cross to tie the game 1–1; he later converted a penalty in the resulting shoot-out, although Toronto ultimately lost 5–3.

[43] From 10 to 12 March 2014, Bernardeschi was called up to the senior national team by coach Cesare Prandelli as part of an internship to evaluate young players ahead of the 2014 FIFA World Cup,[44] confirmed on the next meeting between 14 and 15 April.

[45] Bernardeschi received his first official call up to the Italy senior squad by manager Antonio Conte in March 2016 for friendlies against Spain and Germany.

[46] He made his international debut for Italy on 24 March, coming on as a substitute in a 1–1 home draw against Spain, and was involved in Lorenzo Insigne's goal.

[52] On 6 July, following a 1–1 draw after extra-time against Spain in the semi-final of the competition, Bernardeschi converted his spot-kick in an eventual 4–2 penalty shoot-out victory, to send Italy to the final.

[53] On 11 July, Bernardeschi won the European Championship with Italy following a 3–2 penalty shoot-out victory over England at Wembley Stadium in the final, after a 1–1 draw in extra-time; during the match, he replaced the injured Federico Chiesa late on in the second half, towards the end of regulation time, and later scored Italy's fourth spot-kick (which ended up being the game-winning penalty after teammate Jorginho and England's Jadon Sancho and Bukayo Saka all missed their spot-kicks) in the shoot-out.

[54][55] A quick, strong, creative, technically gifted, and hard-working player, with a good positional sense and an eye for goal, Bernardeschi was regarded as one of Italy's most exciting and talented prospects.

[79] Due to his technique and elegant playing style, Bernardeschi has been nicknamed Brunelleschi, as a reference to the famous Italian Renaissance designer and architect from Florence.