In 1996, Dudek was signed by Feyenoord Rotterdam. The first year, he was second goalkeeper, behind the popular Ed de Goey, but when the latter left a year later to Chelsea FC, the Feyenoord management put confidence in Dudek by not signing another keeper, and from 1997 onwards he was their consistent first-choice in goal.

Signed by Liverpool on August 31, 2001 as a replacement for Sander Westerveld, Dudek also plays regularly for the Polish national team. Despite an impressive debut season in the English Premier League, he suffered a stressful 2002 FIFA World Cup. Dudek was then dropped from the Liverpool team after several goalkeeping errors, particularly two howlers against Manchester United on December 1, 2002. Although he regained his place in the team after Chris Kirkland suffered an injury, he finally lost his position as Liverpool's first-choice keeper after the arrival of Jose Reina in July 2005.

On 25 May 2005, Dudek became an instant hero in Liverpool after a characteristically mercurial performance in the Champions League final in Istanbul against A.C. Milan. Dudek made an incredible double save in the dying minutes of extra-time to prevent Milan striker Andriy Shevchenko from scoring what would almost certainly have been the match winner. Dudek then helped win the trophy for Liverpool with two saves in the penalty shoot-out. Prior to each of the Milan penalties, on the advice of Jamie Carragher, Dudek performed a variety of movements in an attempt to distract the penalty takers. This has since been known as the "Dudek dance", which inspired a dance track called Du the Dudek that was released in July 2005 by the Liverpool-supporting Trophy Boyz. During the post-match interview, Dudek stated that his flamboyant approach to the penalty shoot-out had been influenced by Bruce Grobbelaar, a former Liverpool goalkeeper. Grobbelaar was the hero of the 4-2 penalty shoot-out victory over A.S. Roma in the 1984 European Cup Final (the former name of the Champions League) after provoking Francesco Graziani to miss by wobbling his legs in mock fear. Speaking just after the final ended, Dudek stated in his inimitable English, "I am in the heaven".

After the European Cup final, Dudek was replaced in the first team by Spanish keeper Pepe Reina. Although he went on to make appearances for the Reserves and in Cup competitions, he has rarely featured for the first team since. He did, however, appear in three Premiership matches when Reina was suspended after his red card following a fracas with Chelsea's Arjen Robben. He also played in two more Premiership games towards the end of the 2005/06 season. The next season, injury prevented Dudek from playing in what would have been his final match for the club against Charlton Athletic (also Robbie Fowler's last game) on the final day of the 2006/07 season.

On May 30, 2006, during the friendly match between Poland and Colombia, the crowd in the stadium started to chant the name of Dudek, as a way to express their desire to have the goalkeeper in the 2006 World Cup Squad. This was mainly because of the mistake made by Tomasz Kuszczak, allowing the Colombian keeper Luis Enrique "Neco" Martinez to score a goal from a long punt.

On June 21, 2006, it was reported that Dudek had been left "devastated" by a burglary at his Wirral home, in which the accumulated memorabilia of his career, including his Champions League winners' medal and the shirt he wore in Istanbul, was stolen. The haul, however, was later recovered, and a man and woman charged with the burglary.

On 12th July 2007 it was announced that Jerzy Dudek had agreed to join Real Madrid on a free transfer from Liverpool. As of July 20th, the deal is to be completed as Dudek has passed his medical at Real Madrid. Real Madrid's Club Doctor, Alfonso Del Corral said " Dudek is 34 years old but his health is fantastic and as good as a younger player. He is a true athlete."