Full-time from The Den
Hunt was on hand to capitalise on hesitancy in a new-look Lions rear-guard, scoring twice in the opening 14 minutes to put Mick McCarthy's charges in a commanding 2-0 lead.
But Magaye Gueye reduced the arrears three minutes before the break. Despite a gallant effort in the second-half, Millwall were unable to level and Ipswich sub Jonathan Parr made the points safe with the visitors' third goal 13 minutes from time.
Ian Holloway wielded the axe following the debacle at Bradford City on Wednesday night, making eight changes to the team that started the FA Cup Replay, including handing the captain's armband to defender Sid Nelson, just 17 days after his 19th birthday.
In came right-back Shaun Cummings and Diego Fabbrini for their Millwall debuts, whilst fellow new signings Dan Harding and Stefan Maierhofer made their first appearances at The Den having featured at Blackpool last weekend as The Lions starting XI showed eight changes in all.
It was a brave and it was a bold team selection, but as far as boss Ollie was concerned, the wholesale changes were needed in a bid to address a slump in form and loss of confidence that had seen his team win just twice of their previous 20 matches.
Almost regardless of the result against Ipswich, the manner of the display - win, lose or draw - was always going to be crucial to Lions fans, who like the manager, were left bewildered and embarrassed at the ease with which Bradford brushed aside the team midweek.
Millwall nearly got off to a dream start when debutant Fabbrini's stinging shot flew narrowly wide after his initial effort had been blocked by Christophe Berra.
But hopes of a morale-boosting early breakthrough by the home side were dashed when Town's Hunt was picked out by his brother Stephen Hunt on the left and drilled home a low angled shot beyond the reach of keeper David Forde with just five minutes on the clock.
The Lions persistence was rewarded three minutes before half-time when Gueye grabbed the home team a lifeline, finding space inside the box to fire into the bottom corner.
Gueye sent a 25-yard free-kick inches over the bar and then picked out Byron Webster with a pinpoint corner, but the big defender planted his header agonisingly wide of the upright.
That goal really knocked the stuffing out of The Lions and McCarthy's men comfortably saw out the remaining quarter of an hour to claim all three points.
Scorer: Gueye (42mins)
Ipswich Town: Bialkowski, Mings, Chambers, Smith, Berra, Murphy, Anderson (Clarke, 88mins), S. Hunt (Parr, 64mins), N. Hunt (Sears, 63mins), Bru, Tabb. Subs not used: Crowe, Stewart, Ambrose.
Scorers: N.Hunt (5, 14mins), Parr (77mins)
Att: 11,063 (away 2,503)