Cudicini started his professional career at Serie A side AC Milan in 1992, but struggled to break into the first team and was loaned to Como before moving to Prato and then Lazio in 1996.

Cudicini left Chelsea in January 2009, having made 141 league appearances for the club, and joined local rivals Tottenham Hotspur.

Cudicini made only two appearances for AC Milan (1992–95) in the Champions League, one in the Coppa Italia and none in Serie A during that period in the club's history.

He was loaned to Como for a season in 1993–94, and was subsequently transferred to Prato in 1995, and then to Lazio in 1996 where he suffered a serious wrist injury, and consequently only made one senior appearance.

[2] He made his Chelsea debut on 25 August 1999 in a goalless draw away to Skonto Riga of Latvia in the UEFA Champions League, with the London-based club winning 3–0 on aggregate and advancing into the group stage of the competition for the first time; he came on as a substitute for Ed de Goey with 12 minutes remaining.

[11] On 8 May 2004, Cudicini saved a penalty from Manchester United's Ruud van Nistelrooy, before making a mistake and allowing the same player to equalise.

[2] On 14 October 2006, in a league game against Reading, he was knocked unconscious and had to be stretchered off the pitch while wearing an oxygen mask after coming on as a substitute for first-choice goalkeeper Čech.

However, after returning to action in Chelsea's 2–0 defeat to Liverpool at Anfield in late January 2007, Čech kept both Cudicini and Hilário out of the first team.

He played against Leicester City in a 4–3 win at Stamford Bridge in the next round before making his first appearance of the season in the Champions League, coming on as a substitute against Schalke 04.

Cudicini then featured in the next five games due to Čech's injury, conceding just one goal in the process, against Everton at Stamford Bridge in a 1–1 draw.

He played his last game for Chelsea at home in the FA Cup third round tie with Southend United which ended in a 1–1 draw.

He did not play again for Spurs in the 2008–09 season after the 1–2 victory over Hull City at the KC Stadium a week before the 2009 Football League Cup final.

Cudicini made his first competitive appearance in nearly six months for Tottenham when he came on as a substitute for the injured Heurelho Gomes in a 5–1 victory over Hull City on 19 August 2009.

On 25 August 2010, Cudicini saw his first official action for the club in nearly a year as a half-time replacement for the injured Gomes in the second leg of Tottenham's UEFA Champions League play-off round tie against Young Boys of Switzerland.

[23] He was an eighth-minute replacement for Luka Modrić after Gomes' sending-off against Inter Milan on 20 October, in a 4–3 loss to the reigning European champions at the San Siro.

His final appearance for the club was in a 0–3 win against Carlisle United at Brunton Park in a third round League Cup tie on 26 September 2012.

He was not eligible for England because FIFA Statutes stipulate that the player needs to have held a British passport at the time when he represented Italy at the U16 European Championship, and would have required five years of education in Britain before turning 18.

[46] In August 2019, Cudicini had been appointed technical coach for the players on loan from other clubs, following Eddie Newton's move to Frank Lampard's backroom staff.

[47] In December 2022, Cudicini received his UEFA Pro License in Dublin after attending the FAI Coach Education Department course.