But despite those achievements and his massive standing in the global game, a former Bok prop believes the time has come for Smit to be dropped from the national side.
Smit could do nothing to prevent Saturday's heavy defeat to Australia in Sydney and Ollie le Roux was scathing in his criticism of the veteran front rower.
"John Smit was dreadful," le Roux, who played against the Lions in 1997, told Sport24 when asked about the skipper's performance against the Wallabies.
"I can't think how one could even contemplate taking him to the World Cup."
But while opinions matching le Roux's are becoming more commonplace having been unthinkable two summers ago, the chances of Smit being left at home when the latest global gathering starts in September are still slim to none.
Springbok head coach Peter de Villiers still sees Smit as the man to lead the Boks in the defence of their World Cup crown despite an apparent dip in his form.
Chilliboy Rapelle and Adrian Strauss are the other two hookers in the Bok squad for the away leg of the Tri Nations, with de Villiers unable to find a place for Saracens star Schalk Brits despite him being one of the standout performers in the Aviva Premiership over the past two seasons.
Smit seems certain to start this Saturday's clash with New Zealand in Wellington where he will win his 105th Test cap and continue his reign as the world's most-experienced national captain.