The Spurs midfielder, now on loan at Wolves, scored the second after substitute George Ndah had netted his first goal in 30 months.
Romanian striker Viorel Ganea added the third to condemn Derby to their heaviest defeat of the season and their fourth in five games.
Such a convincing victory did not look likely during an error strewn first half in which both teams conceded possession alarmingly.
The closest anyone came to a goal was when Marcus Tudgay headed a Seth Johnson corner against the crossbar shortly after the striker had almost set-up Tommy Smith.
But the second half belonged to Wolves who took control after Derby centre-half Michael Johnson left the field with a calf injury.
The introduction of Ndah gave Wolves some presence in attack and in the 68th minute the striker powered a header from a corner into the net via Peter Whittingham on the line.
Derby's hopes of getting back into the game were ended by the impressive Huddlestone who played a clever one-two with Ganea before side-footing past Lee Camp from 10 yards.
Huddlestone had failed to score for Derby in 95 appearances but that goal settled the contest and Ganea completed an excellent night for Wolves four minutes from the end when he evaded two challenges before driving a shot into the roof of the net.
The damage could have been even heavier for Derby who were caught out yet again a minute from the end by a cross from the Wolves left that picked out Ki-Hyeon Seol but the midfielder headed straight at Camp.
There were five minutes of stoppage time but most of the Derby fans had long since headed for the exit while the Wolves supporters celebrated a comprehensive victory.