The game was won by Keith Andrews' close-range finish with 21 minutes remaining, but Town had been the inferior side before the goal with managerless Pompey wasting a string of chances.
Ipswich goalkeeper David Stockdale was their stand-out performer as he denied Luke Varney and David Kitson while Liam Lawrence and Dave Norris, a former Town player, also missed good opportunities.
But Andrews' strike, his fifth of the season, proved decisive and Paul Jewell's men held on to stretch their unbeaten run to six games, remaining on the play-off trail.
For Portsmouth, who were led by caretaker duo Stuart Gray and Guy Whittingham, it was a third defeat in four league games and finding a permanent replacement for Steve Cotterill, who left to join Nottingham Forest last week, must be a priority for the south-coast club.
Ipswich came into the encounter with momentum and they were close to taking an early lead when Lee Bowyer's shot and turn from the edge of the area forced Stephen Henderson into a smart save.
Portsmouth were by no means passengers in the game, though, as it flowed from end to end and Stockdale produced a fine save to deny Pompey's Varney after a quick break.
In fact, Pompey began to assume control and they created two further chances to open the scoring but Kitson fired wide and Ricardo Rocha headed straight at Stockdale, both from Lawrence corners.
The half-time interval did not bring a change to proceedings and it was a familiar story in the second period with Lawrence completely missing the ball from five yards out with the goal gaping.
Stockdale again proved an immovable force in the Ipswich goal soon after as he denied Kitson's scrambled shot before Norris dragged the rebound wide from the edge of the area.
However, Pompey were made to pay the ultimate price for not taking their chances as they fell behind in the 69th minute to just Ipswich's second shot on target.
Carlos Edwards whipped a cross in from the right and after Nathan Ellington failed to get a clean header on goal, the ball fell for Andrews who finished with ease from inside the six-yard box.
It was a bitter blow for the visitors and Joel Ward's curling effort from distance, which flew just over the bar, and a misplaced free header from Varney, were further missed chances as they searched for a way back into the game.
It was not to be, though, and Jewell's men were able to celebrate a victory that they barely deserved.