He is best known for his role alongside Franco Baresi, Paolo Maldini, and Mauro Tassotti, forming one of the greatest defences in Serie A and European football during the late 1980s and 1990s, under the success of managers Arrigo Sacchi and Fabio Capello.

Milan would go on to win the match 1–0, as well as the Serie A title, but Costacurta received limited playing opportunities that season, due to the presence of the more experienced Filippo Galli in his position.

[7] The 1988–89 season would see Costacurta gain more playing opportunities and appear more frequently for the club, as he would feature in Milan's 3–1 win over Sampdoria in the 1988 Supercoppa Italiana.

He would make 26 appearances in Serie A that season, and would also win his first European Cup title after Milan defeated Steaua București 4–0 at the Camp Nou, Barcelona.

[7] During the 1989–90 Season, Costacurta won his second consecutive European Cup with Milan, defeating Benfica 1–0 in the final in Vienna, and starting the play which led to Frank Rijkaard's match-winning goal.

[8] He also featured in Milan's Intercontinental Cup win in Tokyo over Atlético Nacional, and in the European Supercup victory over Johan Cruyff's Barcelona.

[7] Following Capello's departure after the 1995–96 title win, as well as the aging and retirement of certain key players, Milan faced dark times in their history.

However, Costacurta, through his joint leadership in defense alongside Maldini, would help Milan reach the 1998 Coppa Italia final, losing out to Lazio despite 2–0 lead on aggreagate.

At the end of the season, Milan managed to capture their 16th Scudetto win, and Costacurta's sixth in total, finishing ahead of Lazio by a single point.

Ancelotti's arrival and several new signings would bring about a new era of European and Italian dominance for Milan, and Costacurta would form part of another excellent defence, which included players such as Maldini, Alessandro Nesta, Jaap Stam and Cafu.

[7] At the end of the season, in 2002, Costacurta's contract was expiring – he therefore decided to leave the club at age 36 following their American exhibition tour in the summer to pursue a Master's in Economics in the United States.

[18] However, Milan lacked defenders in their squad due to injuries, and Adriano Galliani recalled Costacurta to renew his contract the night before the second leg of their crucial UEFA Champions League playoff match against Czech side Slovan Liberec.

At half-time, Milan were leading 3–0, but Liverpool made a second half comeback, scoring three goals to tie the match and send it into extra time.

Costacurta's record was later broken by Marco Ballotta, who on 11 December 2007, played a match at age 43 years and 253 days for Lazio against Real Madrid.

He made his final home start in Milan's 3–2 loss to Udinese on 19 May 2007, converting a penalty that marked his first Serie A goal since the 1991–92 season (15 years after his left-footed volley against Roma on 3 November 1991), and left the pitch near the end of the match to a standing ovation.

[25] A mainstay in the Italy national team throughout the 1990s, Costacurta played for his country in three major tournaments: the 1994 and 1998 World Cups, as well as Euro 1996.

He later became a regular first-team member under his former Milan coach Arrigo Sacchi, who replaced Vicini in 1991 after Italy failed to qualify for Euro 1992 in Sweden.

[28] Costacurta started in Euro 1996 for Italy, as they were eliminated in the first round, in a group with the two eventual finalists, the Czech Republic and Germany.

[25] Costacurta is regarded by many pundits, managers and players as one of the greatest defenders in history; he formed some of the most formidable defensive units of all time during his extensive career at Milan, alongside Paolo Maldini, Franco Baresi, and Mauro Tassotti in particular, but also other top defenders such as Filippo Galli, Christian Panucci, Alessandro Nesta, Cafu and Jaap Stam.

[17][32][33] Costacurta was a tactically versatile defender who excelled anywhere along the backline, which allowed him to have a long and highly successful career, both at club level and with the national side, winning many trophies.

[3][32][33][34][35][36][37][38] Costacurta was a complete, hard-working and experienced defender who was also gifted with good distribution and crossing ability, as well as a solid technique and first touch, which he developed further as his career progressed, despite not initially being the most naturally skilful player on the ball; this enabled him to be comfortable in possession, carry the ball forward into midfield, and start attacking plays from the back-line.

He was a tenacious yet disciplined defender with fast reactions who was known in particular for his exceptional tactical intelligence as well as his timing and strong, precise tackling ability.

[7][17][34][36][39][40][41][42] He was also quick-thinking, mobile, effective in the air, and had an outstanding ability to read the game and anticipate plays, despite his lack of notable pace, physical strength or athletic attributes, due to his slender build.

[53] On 27 October 2008, Costacurta was unveiled as new coach of Serie B promotion candidates Mantova, then 13th in the table, following the dismissal of previous boss Giuseppe Brucato.