Town's new £1.3m record signing Nahki Wells enjoyed a dream debut as Ian Holloway suffered defeat in his first match as Millwall manager.
The Bermudian hot shot, signed from rivals Bradford yesterday, came on as a second-half substitute, and fired in a 90th-minute winner.
Holloway, appointed last Monday, made sure his team got plenty of men behind the ball, and it looked like he was going to claim a point in the battle against relegation from the Championship.
But Wells, who shot in on the angle as visiting defender Jack Smith lopped an attempted headed clearance up into the air, made sure he grabbed the headlines.
Town manager Mark Robins kept the same starting side on duty for the 3-2 FA Cup win at Grimsby while Holloway made just once change after Millwall's 4-1 third-round loss at Southend, Scott McDonald coming in for the suspended Jermaine Easter.
It was a return to familiar territory for the experienced Aussie international and ex-Celtic player, who had a loan spell at Town from Southampton back in 2002 and scored three times against them for Middlesbrough last season.
Town, as usual starting with a 3-5-2 formation, had the first effort on target through Danny Ward, who played a one-two with Jonathan Hogg and tested keeper David Forde with an awkward deflected shot in the fifth minute.
The home team almost played themselves into trouble when Adam Clayton was sold a touch short by keeper Alex Smithies' pass, but the midfielder got back well to make a crucial penalty-area challenge on Lee Martin, who had seized possession.
With the home supporters growing a little restless with their team's sluggish start, Millwall's on-loan Leeds striker Steve Morison broke through in the 22nd minute, but could only produce a daisy cutter of a shot which was easily gathered by Smithies.
As Town found more incision towards the end of the first half, Martin Paterson was twice thwarted by Forde at close quarters, with Ward putting his follow-up effort wide from the second of them.
However Millwall could have gone ahead just before the break, when McDonald rapped a low shot against Smithies' left-hand post before the keeper saved Morison's close-range header as the ball was played back in.
Town's Adam Hammill came close when he flashed a shot across the face of goal early in the second half while Robins made a double change on 55 minutes, bringing on new boy Wells and Duane Holmes for Ward and Hogg.
Millwall substitute Andy Keogh flashed an angled effort wide in the 68th minute, but it was still Town doing the bulk of the attacking, although the stubborn visitors looked relatively comfortable in dealing with the home threat - until Wells made his mark.
