Having survived a bout of testicular cancer as a teenager, Cruden's rise to the All Blacks was meteoric. He led the 'Baby Blacks', New Zealand's Under-20 side, to victory at the Junior World Championship in 2009 and was later named IRB Junior Player of the Year. He played a season of NPC rugby with Manawatu later that year with his name already mentioned in the same breath as the All Black No.10 jersey. While his Test shot did not materialise that season he showed strong form in his first Super 14 for the Hurricanes, winning an international call-up for June Tests against Ireland and Wales. With the Chiefs' Stephen Donald and Mike Delany out with injuries he was immediately elevated to the status of understudy to Dan Carter, playing all three Tests and scoring his first try against Wales in Hamilton. He started his first Test away to Australia later in 2010 following Carter's decision to undergo ankle surgery.

The fly-half signed for the Chiefs during the summer of 2011 and was included in Graham Henry's training squad for the Tri-Nations. However he lost out to Highlanders playmaker Colin Slade as Carter's understudy. Cruden was similarly left out of New Zealand's original 30-man World Cup squad but when New Zealand's biggest fear manifested and Carter was ruled out of the tournament with a groin injury, he was called up as an injury replacement.

Cruden was quickly pressed into action as replaced Slade in the quarter-final against Argentina. Cruden impressed against the Pumas and then out-played Australia playmaker Quade Cooper in the semi final. Although his participatin in the final was cut short by a knee injury, the All Blacks went on to defeat France to claim the Rugby World Cup for the second time.