A brace of own goals from Shane Lowry (63mins) and Mark Beevers (83mins) coupled with a cracking header from Tommy Smith condemned Millwall to a second successive Championship defeat at Portman Road.
Ironically having dominated for the first-half, it was Millwall who looked the sharper side with the score at 0-0 just past the hour mark.
Moments after Richard Chaplow had headed narrowly wide with The Lions best chance of the game left-back Lowry unfortunately broke the deadlock at the other end, turning the ball into his own net from three yards from Aaron Cresswell's cross.
Smith added a second seven minutes later, outjumping Danny Shittu to emphatically head home Paul Anderon's delivery beyond the reach of keeper Stephen Bywater.
Millwall's misery was complete when, quite incredibly, a second own goal handed Ipswich a 3-0 advantage.
This time the unlucky Beevers could do nothing as Anderson stooped to connect with Elliott Hewitt's cross, but the ball hit the Millwall defender on the shin and trickled over the line.
Millwall manager Steve Lomas had made five changes to the team that played against AFC Wimbledon on Tuesday night, including a debut for QPR loanee Shaun Derry.
The opening half belonged to Ipswich in terms of possession and chances, and it took a smart intervention by keeper Bywater to avert the danger on five minutes when he grabbed the ball at the feet of Town striker David McGoldrick as he broke into the area.
Ipswich should have taken the lead on 28 minutes when Luke Chambers was awarded time and space to connect with a Carlos Edwards' corner, only to plant his header over from four yards.
However it was Millwall who picked up after the break and enjoyed their best spell of the game with Chaplow's half volley flashing across the face of the goal and then sending a header from a Derry cross narrowly off target.
However, The Lions then conceded in the most disappointing of circumstances.
Having seen Chaplow go close with his header, play switched to the other end and when the ball went out of play, having clearly taken a deflection off an Ipswich boot, the subsequent throw-in was awarded Town's way.
Ipswich retained possession and seconds later, Lowry's own goal had put the hosts 1-0 up.
Town doubled their tally on 70 minutes courtesy of Smith's thumping header before Beevers' unfortunate own goal seven minutes from time wrapped up victory for Mick McCarthy's side.
The Lions afternoon was summed up perfectly when subs Scott McDonald and Jermaine Easter were blocked in quick succession and the ball fell to James Henry, who lashed wildly over with the goal at his mercy.
Ipswich Town: Loach, Hewitt, Cresswell (Berra, 85mins), Chambers, Smith, Edwards (Anderson, 63mins), Skuse, Murphy, McGoldrick, Tabb (Tunnicliffe, 63mins), Hyam. Subs not used: Gerken, Veseli, Taylor, Nouble.
Booking: Hewitt (87mins)
Scorers: Lowry (og, 63mins), Smith (70mins), Beevers (og, 83mins)
Millwall: Bywater, Smith, Lowry, Bailey, Shittu, Beevers, Chaplow (Feeney, 66mins), Derry, Morison (McDonald, 72mins), Keogh (Easter, 53mins), Henry. Subs not used: Marshall, Dunne, Robinson, Abdou.
Bookings: Derry (40mins), Morison (45mins)