Stephen Ward successfully came through 75 minutes as he stepped up his comeback as an over-age player in the Under-23s.
But the Ireland international was unable to help the Clarets avoid another Professional Development Leagued defeat as Michael Duff’s men shipped three goals after the break.
Burnley had been the better side in the first half but missed an early penalty through Ntumba Massanka and were punished by two goals in as many minutes with just over an hour gone as the Terriers took control.
Ward has missed the Clarets’ last nine Premier League games with the effects of a knee injury and made a welcome return at Huddersfield’s training ground as he further built up his match fitness.
The left-back eased his way back with a polished showing and his influence helped Burnley enjoyed the better of the opening exchanges.
And they should gave gone ahead after 10 minutes when Massanka was tripped in the box by Romoney Chrichlow-Noble.
However, the Clarets’ striker saw his spot-kick saved by Ryan Schofield and as Brad Jackson looked to pounce on the rebound he went down under another challenge which could have brought Burnley another bite at the cherry from a decent penalty claim.
Massanka was out of luck again 15 minutes later when he seized on a poor back-pass and rounded Schofield before seeing his effort cleared off the line by the impressive Chrichlow-Noble.
And Burnley went close again when a Dwight McNeil corner hit the inside of a post and Ward and McNeil combined well to create a chance for substitute Jamie Thomas, which was again blocked on the line.
The visitors continued to press after the break with a Christian N’Guessan volley from another McNeil corner being deflected just over the bar.
But the game turned after 62 minutes when Huddersfield were awarded a penalty of their own.
Rahis Nabi’s tackle on Town skipper Lewis O’Brien looked to be outside the box but the referee decided otherwise and Alex Pritchard – signed from Norwich City in the January transfer window – calmly slotted home to make it 1-0.
Clarets keeper Conor Mitchell had barely touched the ball in anger but 60 seconds later was beaten again when Dominic Tear followed up from an initial smart save from the Northern Irishman to ram home the loose ball.
The Clarets then faded badly and Town cruised to victory, adding a third goal nine minutes from time when Rekeil Pyke – who started the season on loan at Port Vale – raced through to deliver an assured finish and leave Burnley adrift at the bottom of the northern division.
Burnley: Mitchell, Birch, Clarke, Wilson, Ward (Koiki 74), Bayode (Thomas 20, replaced Wood 74), Nabi, N’Guessan, Jackson, McNeil, Massanka. Subs: King, Younger.
Huddersfield: Schofield, Williams Crichlow-Noble, Edmonds-Green, O’Malley, Booty, Daly, Pritchard (Colville 74), O’Brien, Pyke (Obiero 80), Tear (Mewitt 87). Subs: High, Marriott.