The Saints trailed by eight points at three-quarter time before Wanganeen-Milera helped turn the contest in their favour, helping deliver an 8.8 (56) to 7.10 (52) win.
Saturday afternoon's game, held in perfect, sunny conditions at the MCG, proved a low-scoring affair in front of 41,395 fans.
Wanganeen-Milera was quiet early but was thrown behind the ball and grew into the game, finishing with 33 disposals, 629 metres gained and a wonderful goal.
He pulled up awkwardly with an apparent left leg issue early in the fourth but waved away the trainers and shortly after, teed up goals for both Max Hall and Jack Sinclair.
The South Australian is in demand from both Port Adelaide and Adelaide, though St Kilda CEO Carl Dilena told 3AW radio he was "optimistic" the Saints could keep hold of him.
Marcus Windhager had 24 disposals to halftime and finished with 32.
Jack Sinclair (30 disposals) was also busy alongside Callum Wilkie (29 disposals, 16 marks).
Star Richmond defender Nick Vlastuin was typically imperious behind the ball while the Tigers' midfield shared the load and Rhyan Mansell kicked two goals.
The Saints raced away to an early 20-point lead before Mansell steadied Richmond with a slick finish from a tight angle late in the first term.
St Kilda were celebrating captain Jack Steele's 200th game and former Tiger Jack Higgins' 100th AFL appearance as a Saint.
There was a quirky moment when St Kilda ruckman Rowan Marshall gave away a free kick for taking Kamdyn McIntosh's head band off him midway through the second quarter.
Wanganeen-Milera delivered a spark when he pounced on a loose ball, broke a tackle then snapped towards goal, with the ball taking a wicked bounce to sneak through for a major.
The Saints led by four points at the main break and butchered a couple of early opportunities in the third quarter, before McIntosh snapped Richmond in front.
Tim Taranto kicked a marvellous long-range goal just before the three-quarter time siren to deliver an eight-point lead.
The final quarter proved an arm wrestle, but the Saints were more composed when it counted, with McIntosh penalised for running too far as he attempted to launch a late Tiger attack.
St Kilda (8-13) play Essendon at Marvel Stadium next Friday while Richmond (5-16) face fellow cellar dwellars North Melbourne in Hobart on Sunday.