Australia, captained by Aaron Finch, play three games against the Proteas starting on November 5 in Adelaide, with Dunk among a host of fresh faces in the 13-man squad.
With regular wicket-keeper Brad Haddin among those still in the United Arab Emirates on Test duty against Pakistan when the T20 series begins, Dunk leapfrogged other potential glovemen including Tim Paine and former Australian keeper Matt Wade.
His elevation follows his 229 not out in a record domestic one-day innings for Tasmania on Saturday.
"The squad itself includes a good blend of youth and experience, providing Aaron with multiple options with both bat and ball," said national selector Rod Marsh.
"We've seen some good form recently from players such as Cameron White, Nathan Reardon, Ben Dunk and Ben Cutting and they've been rewarded for those good performances,” he added.
"Shane Watson also returns from injury and we certainly know the destruction he is capable of causing in this format of the game,” he said.
All-rounder Watson has not played since the Indian Premier League (IPL) in May after being ruled out of Australia's tours of Zimbabwe and the UAE with complications from stepping on a ball during training.
He made his return in a Sydney club match on Sunday, with the break allowing him to work on his fitness and strength.
As well as Dunk, Queenslander Reardon is in line for his international debut, while selectors have shown faith in promising youngsters Sean Abbott, Cameron Boyce and Pat Cummins to continue their development.
Nic Maddinson returns to the squad and will likely open the Australian batting alongside Finch, while veteran left-arm paceman Doug Bollinger has been given another chance at age 33.
After Adelaide, the series moves to Melbourne and Sydney with the squad coached by Trevor Bayliss while Darren Lehmann is on Test duty.

The squad:
Aaron Finch (capt), Sean Abbott, Doug Bollinger, Cameron Boyce, Pat Cummins, Ben Cutting, Ben Dunk, James Faulkner, Nic Maddinson, Nathan Reardon, Kane Richardson, Shane Watson, Cameron White.

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