David Wagner’s side faced fellow promotion hopefuls Reading at the John Smith’s Stadium.
With Aaron Mooy one of several players returning to the starting line-up against the Royals, the Terriers passed up the opportunity to take a first half lead when Rajiv van La Parra saw his penalty saved.
In front of almost 20,000 fans, the game appeared to be heading for another goalless draw when Philip Billing pounced from close range on 82 minutes to send the home fans wild.
It proved to be the only goal of the game and put Huddersfield within three points of an automatic promotion berth in the Championship.
It was the Terriers’ 11th win in 13 league matches with their excellent form showing no signs of abating.
Last weekend, Huddersfield made the short trip to Oakwell to face Yorkshire rivals Barnsley who retain interest in sneaking into the play-off spots.
The hosts, however, were outplayed for much of the game and had their goalkeeper Adam Davies to thanks for keeping them in the game.
Even he, however, was powerless to stop Michael Hefele’s thumping header on 18 minutes with Mooy inevitably supplying the cross.
The Tykes improved after the break, but it looked like the visitors would take all three points until the 75th minute when Marley Watkins levelled for Barnsley, earning Paul Heckingbottom’s side an underserved 1-1 draw, though the Terriers went close to scoring again several times in a frantic finale.
It proved a costly two points dropped for Huddersfield, following Newcastle’s surprise 2-2 draw with struggling Bristol City.
Brighton beat Reading 3-0 to return to the top of the Championship with the leaders meeting Newcastle on Tuesday evening as the title race enters the final third of the campaign.
Huddersfield are third, five points adrift of Newcastle and will perhaps be hoping Brighton take all three points with Wagner’s side hosting Rafa Benitez’s side this weekend for what could be a pivotal clash.
Wagner’s touchline spat with Leeds United boss Garry Monk earlier this month means he will have to watch the replay against City from the stands as he serves the first of a two match ban.
Huddersfield remain unbeaten in their last nine games in all competitions and have won six of their last eight games on the road – City have won seven of the past 10 matches in all comps and are unbeaten in the last seven games.
The winners also now know they will face Middlesbrough away in the FA Cup 6th round.