Ed Upson scored his first goal for Millwall but a Nahki Wells brace either side of half-time ensured that The Lions had nothing to celebrate at the end of 90 frustrating minutes at the John Smith's Stadium.
Wells opened the scoring for Huddersfield after 37 minutes with a super strike, only for Upson to haul The Lions level with an equally sweet finish just four minutes later, thumping home a half-volley from 12 yards.
Former Bradford City striker Wells fired Huddersfield 2-1 ahead on 56 minutes from the penalty spot after Nicky Bailey was penalised for a foul and Chris Powell's side were rarely troubled thereafter as Ian Holloway's men crashed to their fourth defeat in five games.
Holloway was forced to shuffle his defensive pack, starting with the same back four that finished the 0-0 draw against Nottingham Forest with a start for Jimmy Abdou at right-back in Carlos Edwards, sidelined until next year with knee ligament damage sustained early in that game.
Bailey made a welcome return to the first team, making his first start of the season in a midfield three that included Shaun Williams and Upson. Up front Ricardo Fuller was flanked by Scott McDonald and Martyn Woolford in a 4-3-3 formation.
Huddersfield, looking for their first win since 19th August - and first since manager Chris Powell took charge three games ago - boosted their ranks hours before kick-off with the emergency loan signing of striker Grant Holt, so often a thorn in The Lions' side during his days as a Norwich player.
The two teams kicked off both determined to end their respective win-less runs, but the opening exchanges proved to be scrappy with no real scoring chances created, although Abdou did get two crosses into the danger zone in quick succession, neither of which really troubled the home defence.
Town's Wells twice had the ball in the back of the net, on both occasions moments after the whistle had blown for a foul and off-side, with referee Carl Boyeson losing patience and brandishing a yellow card on 23 minutes following the second indiscretion.
The Lions earned their first corner of the game after 28 minutes and seconds after Upson's delivery was cleared, the ball was played back in Abdou and Upson's sweetly struck curling effort sailed over keeper Alex Smithies and smacked against the upright.
Williams had an 18-yard drive deflected for a corner and Smithies did well to punch Woolford's inswinging delivery away from goal.
The game finally exploded into life eight minutes before half-time with Town breaking the deadlock and Millwall responding just three minutes later.
Town's opening goal was literally a bolt out of the blue - a sublime half-volley from the edge of the area by Wells after Harry Bunn had played the ball into his path. It was certainly a shock as the home side had offered little as an attacking threat up until that point.
However the celebrations were cut short barely four minutes later when a nice passage of play involving Abdou and McDonald saw the latter slip the ball to Upson, who matched Wells' effort with a stunning half-volley that gave Smithies no chance.
Millwall had keeper Forde to thank for a smart save to block Wells' goal-bound shot on the stroke of half-time, beating away the stinging strike as it arrowed towards the bottom corner.
Wells, who scored on his debut for Huddersfield against Millwall last season, was not to be denied when Town were awarded a 56th-minute penalty when Bailey was penalised for bringing down Bunn. The Millwall man's protests earned him a booking, whilst Wells tucked home the resulting spot-kick to put the home side 2-1 ahead.
Huddersfield introduced Holt looking for a third, killer, goal and the sub twice went to ground within minutes of entering the fray, first following an off the ball incident and then under pressure from Mark Beevers.
Millwall defender Beevers was denied an equaliser with 20 minutes remaining when he picked up Wollford's corner and hit a fierce effort that was brilliantly tipped away by Smithies at full stretch.
Holloway made a triple substitution just moments later, bringing on Justin Hoyte, Mathias Ranegie and Magaye Gueye for Upson, Woolford and Bailey. Hoyte slipped in at right-back enabling Abdou to revert to his usual midfield role, with Geye and Ranegie adding fresh legs up front.
Ranegie's neat flick set up Fuller with nine minutes remaining, but the striker dragged his effort wide from 14 yards as The Lions tried to build up a head of steam.
The Ranegie-Fuller combination caused problems for a second time on 87 minutes when Ranegie's deep cross was headed wide, but Millwall were unable to create any period of sustained pressure as the home side comfortably saw out the remainder of the game, including five minutes of injury-time, to leave The Lions without a win in four games.
Huddersfield Town: Smithies, Hudson, Hogg (Scannell, 85mins), Butterfield, Coady, Robinson, Wells (Wallace, 90+2mins), Smith, Bunn, Lynch, Peltier (Holt, 64mins). Subs not used: Murphy, Dixon, Ward, Stead.
Bookings: Wells (23mins), Smith (53mins)
Scorers: Wells (37mins, 57mins pen),
Millwall: Forde, Abdou, Malone, Dunne, Beevers, Bailey (Ranegie, 73mins), Edwards, Upson (Hoyte, 74mins), McDonald, Fuller, Woolford (Gueye, 74mins). Subs not used: King, Webster, Gregory, Chaplow.
Bookings: Bailey (56mins), Beevers (68mins), Ranegie (78mins) Dunne (81mins), Williams (89mins)
Scorer: Upson (41mins)
Ref: C. Boyeson