Smit played his first Springbok game in 2000 at the age of 22, when South Africa beat Canada 51–18 at Basil Kenyon Stadium in East London. Between October 2003 and June 2007, Smit played in a record 46 consecutive Test matches for South Africa, though it was not until 2004, when he was made captain of the squad by then new coach Jake White, that he became a regular member of the starting XV. Smit's record-breaking sequence of appearances came to an end with South Africa's first match of the 2007 Tri Nations, against Australia, when he suffered an injury that prevented him taking any further part in the tournament. He recovered from his injury in time to take part in the 2007 Rugby World Cup, in which he started in 6 out of 7 South African matches and in which his leadership qualities came to the fore, saw South Africa win the William Web Ellis Trophy for the second time. When Peter de Villiers was appointed as the new South Africa coach in 2008, one of his first decisions was to re-appoint Smit as the captain of the national side. Smit led South Africa in their opening game of the 2008 Tri Nations, against New Zealand in Wellington, but suffered a groin injury when he was lifted and dumped by New Zealand lock Brad Thorn after the whistle had blown: Thorn received a one-match suspension but Smit missed the rest of the tournament, being replaced as captain by veteran Springbok lock, Victor Matfield. In 2009, Smit led South Africa to a series victory against the visiting British and Irish Lions, and followed this by leading his team to success in the 2009 Tri Nations, in which South Africa won five of their six matches, including a clean sweep of three wins against New Zealand. In the first test against New Zealand, Smit equalled the record of 59 Tests as captain held by Australia's George Gregan and England's Will Carling. The following week, he became the most-capped captain in international rugby history. As of September 2009, Smit is one of South Africa's most successful captains ever, having led the Springboks to victory in 46 of the 64 games that he captained, a win percentage of 72%. He has won more tests as captain than any other Springbok has played as captain. On 23 August 2010, he played his 100th Test – only the 15th player ever, and second South African to reach that milestone. After his Springbok retirement his record as captain for the most international games was broken, by Ireland's Brian O'Driscoll in 2012 and New Zealand's Richie McCaw in 2013.
During the run-up to the 2007 Rugby World Cup, he was linked with the French club Clermont. He eventually signed a two-year deal with Clermont, effective after the World Cup. Despite his move to France, the South African Rugby Union announced on 20 February 2008 that he would retain his Boks captaincy.. After just one year with Clermont, Smit rejoined the and the Super 14 side Sharks.
2009 British and Irish Lions Tour
Smit captained South Africa in their 2–1 series win over the British and Irish Lions