The Proteas skipper contributed 125 to South Africa's 320 for five but it was Miller's 139 that really caught the eye, a 108-ball assault on the Australian bowlers that featured 13 fours and four brutal sixes.
Dale Steyn kept up the momentum by dismissing Chris Lynn with the first ball of the Australia innings, and his fellow pacemen Kagiso Rabada and Lungi Ngidi soon sent Aaron Finch and Travis Head on their way to reduce their hosts to 39-3.
Shaun Marsh (106) steadied the innings in a fourth-wicket stand of 107 with Marcus Stoinis (63) but once he departed four balls after recording his sixth ODI century, home hopes of only a third win in 14 one-dayers this year faded.
Steyn (3-45) returned to remove Alex Carey for 42, leaving Glenn Maxwell (35) as the last recognised batsman, but he was unable to score quickly enough to challenge the South African tally and Australia finished on 280-9.
"From the batting point of view we were good today but I thought from a 'death bowling' point of view we were excellent," Du Plessis said at the presentation. "It was a great game."
Australia, who bounced back from losing the series opener in Perth by six wickets to beat the Proteas by seven runs in Adelaide on Friday, won the toss and sent the tourists in to bat at Bellerive Oval.
Mitchell Starc and Stoinis combined to remove the first three batsmen for 55 runs but that only served to bring Du Plessis and Miller together for their record stand -- the highest for the fourth wicket by a pair of South Africans.
Miller benefited from a DRS call that overturned an lbw decision when he was on 41 and made the most of what looked like a fortuitous reprieve as he and his captain plundered 130 runs off the last 10 overs, 75 in the last five alone.
Du Plessis's 114-ball innings included 15 fours and two sixes and was his 10th in international one-dayers, while Miller's vindicated his elevation up the batting order.
The same could not be said of Lynn's promotion to opener and Australia still have plenty of question marks over their batting ahead of their defence of the World Cup in England next year.
"Once you get 'in' you can really cash in the back overs here," said Australia skipper Finch.
"Maybe we mis-executed a little bit but they also batted extremely well."
(Reporting by Nick Mulvenney; Editing by John O'Brien and Clare Fallon)
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