Before his first full international cap, Vermeulen represented South Africa at the second level of international rugby, appearing for the
Emerging Springboks. One highlight of his appearances for the Emerging Boks was being in the squad that performed against the
British & Irish Lions, holding them to a 13–13 draw,
during their tour to South Africa in 2009. Vermeulen looked like being a certain selection for the
Springboks, Vermeulen was not called into the Springbok squad that faced
Wales,
Italy and
France. He was also omitted from the Springboks
2010 Tri Nations Series squad. After a stand out Currie Cup domestic Rugby Season, Vermeulen was named as part of the 39-man preliminary training squad ahead of the 2010 end of year grand slam tour to the Northern Hemisphere. He was once again overlooked for selection in the final squad. Vermeulen made his international debut for
South Africa on 8 September 2012, where he formed part of the starting lineup going up against
Australia. He was selected again to start the following week against New Zealand in
Dunedin, where South Africa lost by 10 points. On 29 September 2012, South Africa beat
Australia 31–8, a victory which marked Vermeulen's first Springbok win. He was selected for the Springboks' 2012 Northern Hemisphere tour. Vermeulen received a
man of the match award for his performance against England at Twickenham during this tour, based on a number of vital turnovers on the ground, 15 hard tackles, and his role of primary ball carrier on the day. In 2014, he was one of five nominees for the
IRB Player of the Year award. Vermeulen played in the
2019 Rugby World Cup Final against England. He was part of the South African team that won their third World Cup at the Yokohama Stadium in Japan. He was awarded a man of the match award for his performance where he made a number of vital contributions, including 10 carries, making 49 metres (both the most in the match) and 2 turnovers. Vermeulen was called up by the Springboks at the
2023 Rugby World Cup and the team went on and win the World Cup once again after the
2019. Vermeulen announced his retirement from rugby on 8 November 2023. In November 2025, ahead of the final fixture in the
2025 Autumn Nations Series against
Wales, South Africa head coach
Rassie Erasmus mentioned the possibility of Vermeulen, who had taken up a role as an assistant coach with the team, coming out of retirement in the event of a late injury crisis ahead of the game. No injuries were reported and he did not play the fixture. ==Honours==