Butt started his professional career with modest VfB Oldenburg, achieving promotion to the second division in 1996. He moved to Hamburger SV in the 1997 summer and, in his second season, scored seven goals for the team – all from the penalty spot – adding nine in similar fashion the following campaign.

He won three international caps for Germany in friendly matches, his debut coming against Liechtenstein on 7 June 2000, where he appeared for the second half of an 8–2 routing.

Butt joined Bayer 04 Leverkusen on a free transfer in 2001, being the side’s undisputed starter in the subsequent campaigns (he only missed one Bundesliga match in his first five seasons combined and added seven goals), and appeared in all the games (17) for a team that lost to Real Madrid in the 2001–02 UEFA Champions League final, scoring a penalty in a 3–1 home win against Juventus F.C. in the second group stage.

In 2003–04, after scoring a penalty in an away match against FC Schalke 04 on 17 April 2004, Butt turned away from midfield and began to enthusiastically celebrate with his teammates. He did not notice the whistle for the restart of the game and continued to celebrate. Schalke player Mike Hanke took the opportunity to shoot from the halfway line and scored while Butt was still jogging back to his position.

After losing Leverkusen’s nets to the young René Adler during the 2006–07 season, Butt decided to cancel the contract that linked him to the club until 2009, activating a clause that allowed him to leave the club should he fail to appear in more than half of the games during the second half of the campaign. In July 2007, he signed a two-year deal with Portuguese club S.L. Benfica.

Butt made his Eagles debut in the summer tournament of Torneio de Guadiana, held between Benfica, Sporting Clube de Portugal and Real Betis. In the competition, he saved a penalty against Betis, helping Benfica with the final win. At the Lisbon outfit, however, he played understudy to Portuguese international Quim, being used in the domestic cup matches. He only made one league appearance for Benfica, coming on as a substitute after Quim was sent off against C.S. Marítimo in October 2007 – in this match, he saved a penalty from Ariza Makukula with his first touch of the game, and his team eventually won 2–1.

On 4 June 2008, Butt signed a two-year contract with reigning champions FC Bayern Munich and was expected to act as backup to Oliver Kahn’s heir, highly rated young Michael Rensing. He made his official debut for the club in the Champions League round-of-16 second leg against Sporting Lisbon in a 7–1 home drubbing, on 10 March 2009. With Rensing dropped to the bench following a 5–1 loss at Vfl Wolfsburg, he also started the remaining games of the season, as the initial first-choice was also nursing a hand injury.

After the team’s poor start to the 2009–10 season with Rensing in goal, Butt was reinstated as the first-choice. On 8 December 2009, he scored his first goal for the club, a crucial penalty in the club’s last Champions League group stage match at Juventus, coming from behind to a 4–1 victory – after this feat, he has managed to score a goal against Juventus in the Champions League for all three major German clubs he represented.

On 30 January 2010, Butt missed out on the opportunity to score his first league goal for Bayern as his penalty was saved by 1. FSV Mainz 05’s Heinz Müller, but it proved to be of no detriment to the club as it won 3–0. On 16 February, he was rewarded for an outstanding season with a contract extension until 2011. He was also in goal for the Champions League final, where his team was denied an historic treble after losing 0–2 to Inter Milan.

On 6 May 2010, Butt, Neuer and Tim Wiese were chosen as Germany’s goalkeepers for the 2010 World Cup, with the Bayern man taking the place of former Leverkusen teammate Adler, who had to withdraw due to a rib injury. He made his first competitive international appearance on 10 July, appearing in the 3–2 win against Uruguay in the tournament’s third-place playoff.

Midway through the 2010–11 season, 36-year-old Butt lost his starting place to another club youth graduate, Thomas Kraft. However, a series of unconvincing displays by the youngster, including a 2–3 home loss against Inter Milan in the Champions League quarterfinals on 15 March 2011, and a 1–1 away draw with 1. FC Nürnberg on 9 April, paved the way for the veteran to return to the starting line-up, which happened on 17 April, in a 5–1 home victory over former club Bayer Leverkusen, and he still appeared in 30 official games during the campaign (23 in the league), as his team finished in third position.

On 3 May 2011, Butt signed a one-year extension to his contract with Bayern, backing up newly signed Manuel Neuer. He retired at the end of the season at the age of 38, after a friendly with the Netherlands on 22 May 2012 in which he acted as captain.

Butt was appointed head of the Bayern Munich Junior Team on 1 July 2012. He left the position on 7 August, stating “I misjudged this field of activity, for which I’ve had responsibility for a few weeks now. I approached my new appointment with great enthusiasm, but I have realised that the task does not offer the satisfaction and passion I wanted. This is the reason for my decision. I would like to thank FC Bayern for their understanding.”