The Proteas were struggling on 55-3 when Miller joined Du Plessis at the wicket and the destructive duo took the Australia attack apart with a partnership of 252 - the third highest in ODI history for the fourth wicket.
Miller made an ODI-best 139 from only 108 balls and captain Du Plessis hit a magnificent 125 from 114 after he was dropped by Alex Carey on 29, a blemish that proved to be costly as the tourists posted 320-5.
South Africa took 174 from the last 15 overs and although Marsh (106) and Marcus Stoinis (63) gave Australia hope, they fell short on 280-9 - Dale Steyn (3-45) and Kagiso Rabada (3-40) taking three wickets apiece.
Mitchell Starc (2-57) snared Quinton de Kock caught behind with a peach of a delivery and Stoinis saw the back of Reeza Hendricks in a great start for Australia after Aaron Finch won the toss.
Aiden Markram struck three sixes before he was strangled down the leg side off Starc, but Du Plessis and Miller came to the rescue.
The experienced duo were watchful early in the partnership and the skipper was given a life when Carey failed to take a fourth catch after Glenn Maxwell drew an edge.
Miller successfully reviewed after being given out leg before off Maxwell on 41 and the boundaries started to flow as the clean-striking pair gave an exhibition of exquisite timing.
Du Plessis overtook Miller to bring up his 10th ODI hundred and Miller reached his fifth by ramping Pat Cummins for four in an expensive 47th over.
Miller launched Starc for six over mid-off and Du Plessis struck three consecutive boundaries in a Starc over which cost 20 runs before Stoinis had the captain caught in the deep, having struck two sixes and 15 fours.
The explosive Miller went in the final over from Josh Hazlewood after clearing the ropes four times and hitting another 13 boundaries, Australia left shell-shocked following a brutal onslaught.
Steyn had the promoted Chris Lynn caught behind in the first over and Australia were 39-3 in the 11th with Aaron Finch and Travis Head back in the pavilion.
Marsh and Stoinis put on 107 for the fourth wicket, both batsmen reaching their half-centuries with sixes as they raised the run rate to give Du Plessis plenty to ponder.
Stoinis successfully reviewed after being given out leg before when he got an inside edge on a delivery from Markram, but fell to Dwaine Pretorius (2-61) in the next over.
Marsh continued to strike the ball with great power and reached three figures off 98 balls, but fell to Pretorius in the next over.
Steyn dismissed Carey (42) and Maxwell (35) and Rabada struck twice in the final over as Australia slumped to a fifth successive ODI series defeat.
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