Midfielder Collins, revelling in a new role behind the front two, scored a goal and hit the woodwork but was sent off for two bookable offences.
He was booked early on for a cynical foul but then found himself in the thick of a melee after Joe Skarz and Ryan Smith had clashed.
Referee Darren Deadman spotted Collins in the crowd and issued a second yellow card.
Huddersfield went behind to Darren Byfield's 15th goal of the season after Paul Robinson had flicked on Dave Brammer's corner.
Millwall, unbeaten in four matches, looked good for the first 20 minutes but when Collins fired Huddersfield level, the home side took a grip.
Collins' long ball set up Gary Taylor-Fletcher for a header but keeper Lenny Pidgeley tipped the ball onto the bar.
Midfielder Mark Hudson, who had been told by former manager Peter Jackson he had no future at the club, then helped clinch the points for his new boss.
Luke Beckett thought his perfectly-weighted lob had crossed the line before Robinson hooked it clear but Hudson followed up to lash into the top corner.
Collins then saw his header come back off the underside of the bar before two goals from Beckett sealed it.
Hudson was brought down by Danny Senda and Beckett drilled home the penalty kick.
Beckett's second came six minutes later when he slotted past Pidgeley, the first time Huddersfield had hit four goals this season.
After Collins' sending off, Town lost their momentum and Alan Dunne side-footed home unmarked in the third minute of stoppage time.