The 25-year-old's header earned Mark Robins' side their first win at The Den since 2007, when both sides played in League One.
The Lions are now firmly at the bottom of the Championship and have not scored in the division since April.
Millwall thought they had gone in front in the opening five minutes after Jermaine Easter tucked away a corner, but referee Oliver Langford pulled the play back for a handball by Steve Morison.
Moments later Morison had a great chance to give his side the lead, but the striker was unable to head in James Henry's cross.
Huddersfield had their first chance of the match 13 minutes in after Joel Lynch headed Adam Hammill's free kick wide of the post.
After a long period of possession and chances from the home side, Huddersfield nearly grabbed the lead just before the half hour mark. A long ball forward from Hammill was met by James Vaughan, who got between the Millwall defence but saw his attempted chip stopped by Stephen Bywater.
Millwall responded with a chance of their own soon after, with Morison failing to head Alan Dunne's cross on target.
Ten minutes before half time each side had a great chance to go ahead. Martin Paterson tried to lob the keeper for the Terriers, but Bywater denied the striker brilliantly. Moments later, confusion at the back for Huddersfield allowed Morison to head towards goal forcing Alex Smithies into an acrobatic save.
Just under five minutes into the second half and Millwall had another chance, but Henry's shot flashed across the face of goal.
However 10 minutes later the visitors went ahead. A corner from Hammill was headed in brilliantly by Vaughan for his fourth goal of the season.
Immediately after the goal Steve Lomas substituted Richard Chaplow and Easter, which was met by a volley of boos from the home fans.
After the away side went in front, Millwall began to chase the game but the Terriers kept the majority of possession with neat, little passes across the middle.
The Lions had a great chance to equalise with less than 15 minutes left after Dunne drove in a great low cross across the box, but no Millwall player could get on the end of it.
To add to the further frustration of the Millwall fans, their side's passing seemed to be going astray as the game went into the final stages.
In the final seconds Dunne had a strike from outside the area which was well saved by Smithies.
There was still time for one more chance for the hosts as Nicky Bailey's strike glanced over the crossbar.