Terriers captain Peter Clarke headed home the only goal at the Galpharm Stadium before half-time, while Jonathan Obika nodded Millwall's best chance against the crossbar.
Clear-cut scoring opportunities were scarce and Huddersfield's leading marksman Jordan Rhodes should have done better when steering a shot wide on 38 minutes after fine work from the impressive Gary Roberts.
But, moments later, the hosts grabbed the decisive goal when Lions keeper David Forde misjudged a corner and Clarke rose to head home at the back post.
Theo Robinson had a good chance to increase the Terriers' lead early in the second half, but his lob over the back-peddling Forde was off target.
Substitute Neil Harris almost made an immediate impact for the Lions when his cross was glanced narrowly wide of the upright by Marc Laird.
And on 73 minutes Obika, who was an early replacement for Shaun Batt, should have levelled, but he headed Jack Smith's cross against the bar when picked out unmarked inside the six-yard box.
Millwall, who would have gone back into second with a point, tried to mount a late rally, but Huddersfield held on to open up a six-point cushion over seventh-placed Colchester United.