Vercoutre previously played for Montpellier before moving to Lyon in 2002. In 2004, he joined Strasbourg on loan, but only managed to play eight games for them before returning to Lyon. Due to Grégory Coupet's injury for the 2007 portion of the 2007–08 Ligue 1 season, Vercoutre became Lyon's first choice keeper and played in every game until Coupet's return. During that time, he made a crucial penalty save in the UEFA Champions League against Stuttgart which helped Lyon progress to the round of 16. After the departure of Hugo Lloris to Tottenham Hotspur in August 2012, Vercoutre became the first choice goalkeeper for Lyon. At the end of the 2012–13 season, however, he lost the first-choice place to Anthony Lopes. In June 2014, Vercoutre left Lyon 12 years after his arrival to sign a two-year contract with newly promoted Ligue 1 side Caen.