Gez Sithole scored his first Wanderers’ goal but it wasn’t enough to prevent a losing start to the B team’s Central League Cup campaign.
Sithole slotted home Conor Carty’s cross to halve Town’s lead with 10 minutes to go of their Group A meeting.
But the Whites were unable to find a late leveller as they paid the price for missed chances earlier in the contest as they continue to develop as a team.
Matt Craddock’s side dominated for much of the afternoon at Lostock but goals either side of the break from Terriers’ frontman Charles Ondo gave the Yorkshiremen the points.
Wanderers - with Matty Grivosti prominent following his return from a loan spell at Yoevil Town - should have been comfortably ahead by the break after creating almost all of the openings as they played the first of their four group games in the competition.
Carty – with two goals in his first two Central League games – was a constant threat once he flashed a header from a Craig Stanley free-kick over the bar with 10 minutes gone.
Another Stanley set-piece saw Carty head wide before the former Wolves youngster was unable to get enough on a low cross from Sithole to steer the ball goalwards.
The best chance came, though, when Carty returned the favour for Sithole who couldn’t convert from close-range as he mis-kicked in front of goal.
Town keeper Nicholas Bjlokapic had to save from Carty and the lively Matty Tweedy, while skipper Adam Senior also headed over the top from another Stanley delivery.
And having spurned those chances, Wanderers then found themselves behind two minutes before the break when Ondo broke into the box and steered a shot past Luke Hutchinson.
Bjlokapic remained the busier keep and five minutes into the second half had to make another stop to keep out an effort from Nelson Khumbeni after he had been teed up by the busy Stanley.
But rather than sniffing an equaliser the Whites suddenly found themselves 2-0 down.
Hutchinson had just made a decent stop with his legs to deny Aaron Rowe but was then powerless to stop Ondo doubling his tally when his deflected shot on the turn flew in.
Wanderers looked to respond with another spell of pressure that saw them keep Town penned in.
They finally got their reward when summer signing Sithole slid the ball home but the visitors then held on to sit joint top of the group with Rochdale – opening-day winners over Lincoln City.
Wanderers: Hutchinson; Senior, Toure, Tutte; Grivosti, Khumebni, Tweedley, Conway; Stanley; Sithole, Carty. Substitutes: Yoro, Ahmed, Kamara, Litherland.
Huddersfield: Bjlokapic, Eccleston, Daley, Maroodza, Ayina, Whittingham, Rowe, Diarra, Ondo, O’Brien-Brady, Bright.
Pictures: Kevin Hayden