Jamaican international Paul Hall denied Huddersfield the chance to go second in League One after a two-goal blast.
Hall made it 15 goals for the season with two smart second-half finishes after Huddersfield had run riot in the first 45 minutes.
The Terriers needed to win by two clear goals to return to the second automatic promotion spot and at half-time they were well on course.
On the first-half showing Huddersfield looked like they would grace the Championship but their second-half capitulation summed up their season.
With more consistency Town would have sealed automatic promotion long before now.
David Graham, on loan from Sheffield Wednesday, scored his seventh goal to put Huddersfield ahead but the home side could not press home the advantage.
They were totally dominant in the opening period with Danny Schofield outstanding.
Schofield struck the bar from an acute angle and Graham almost embarrassed keeper Barry Roche with a 25-yard lob.
Roche then made amends with a double save from Chris Brandon and Graham.
Brandon, against his former club, saw his shot beaten out by Roche only for the rebound to drop for Graham but again the keeper got across.
Huddersfield went ahead through Graham in the 13th minute after good work from Danny Adams and Schofield.
The chance to cross seemed to have gone but Schofield produced a piece of magic and Graham gambled at the near post to plant a header past Roche.
Hall and Kevan Hurst had a couple of half chances for the visitors but Huddersfield continued to dominate.
Graham almost grabbed a second when Town skipper Jon Worthington played a delightful little ball into the box and Graham took it in his stride and lashed a volley into the side-netting.
Huddersfield lost right-back Andy Holdsworth at half-time and he was badly missed.
Chesterfield boss Roy McFarland re-organised his side and they were transformed.
Skipper Mark Allott tested keeper Paul Rachubka just two minutes after he fell heavily when making a catch but he clung on.
Huddersfield never recaptured their first-half form and Hall pulled the Spireites level in the 54th minute thanks to a breakaway by Jamie O'Hara.
He slipped a pass to former Huddersfield striker Wayne Allison who fired across goal for Hall to tap home from close range.
Huddersfield never looked like hitting back and Hall grabbed his second when Allott slipped a pass out wide and Hall moved forward and fired past Rachubka.
After that there was simply no way back for Huddersfield.