On 27 August 2011, it was announced NEC and Ajax had reached an agreement for the transfer of Cillessen to the Amsterdam club for an estimated €3 million.
He signed a five-year contract, binding him to Ajax until 2016.

Cillessen made his first appearance for Ajax on 21 September 2011, in a 2nd round KNVB Cup away match against VV Noordwijk.
He played the full match, conceding only to Sijbren Bartlema in the 66th minute of the 3–1 away victory.
He made his first league appearance for Ajax in a 2011–12 Eredivisie match on 23 October 2011 against arch-rivals Feyenoord, coming on as a 66th-minute substitute for right back Gregory van der Wiel, after starting goalkeeper Kenneth Vermeer had been shown a red card.
With Ajax down to ten men, Cillessen helped Ajax retain a 1–1 draw after Jan Vertonghen tied the match just minutes after the ejection of Vermeer.

Cillessen's breakthrough into the first team began during the 2013 pre-season.
Manager Frank de Boer said both of his two leading goalkeepers would get a chance to show why they should be his first choice.
Early in that season, Cillessen made his first sustained run of appearances for Ajax in the Eredivisie.
On 27 August 2011, it was announced NEC and Ajax had reached an agreement for the transfer of Cillessen to the Amsterdam club for an estimated €3 million. He signed a five-year contract, binding him to Ajax until 2016.
Cillessen made his first appearance for Ajax on 21 September 2011, in a 2nd round KNVB Cup away match against VV Noordwijk. He played the full match, conceding only to Sijbren Bartlema in the 66th minute of the 3–1 away victory. He made his first league appearance for Ajax in a 2011–12 Eredivisie match on 23 October 2011 against arch-rivals Feyenoord, coming on as a 66th-minute substitute for right back Gregory van der Wiel, after starting goalkeeper Kenneth Vermeer had been shown a red card. With Ajax down to ten men, Cillessen helped Ajax retain a 1–1 draw after Jan Vertonghen tied the match just minutes after the ejection of Vermeer.
Cillessen's breakthrough into the first team began during the 2013 pre-season. Manager Frank de Boer said both of his two leading goalkeepers would get a chance to show why they should be his first choice. Early in that season, Cillessen made his first sustained run of appearances for Ajax in the Eredivisie.
Jasper Cillessen