The Clarets were unable to find a cure for their untimely bout of home sickness as a second defeat in three games at Turf Moor left them off the play-off pace.
Having been such a force on their own patch for much of the season, the air of invincibility has suddenly deserted Eddie Howe's men as a second-half fightback proved not enough to peg back a two-goal deficit.
With David Norris and Connor Wickham scoring in quick succession either side of the 20-minute mark, the Clarets were left with a Herculean task to try and avoid extending their winless run to four matches.
A much improved second-half performance and Jay Rodriguez's 13th-goal of the season gave them hope.
But ultimately Burnley could not repair the early damage to leave themselves with just eight games to put together the run they need to bridge what is still not an insurmountable gap to the top six.
Howe's team selection hinted at a changing of the guard as, for the first time, none of the players who started the Clarets' play-off final win two years ago kicked off against an Ipswich side playing for neither promotion or for their Championship lives.
David Norris fires Ipswich ahead
But the bright new dawn didn't last long as the Clarets failed to make the most of an up-tempo start.
Good play between Chris Eagles and Dean Marney, captain for the first time, created a chance for Ross Wallace but on his right foot the result was a sliced effort wide of the target.
And Ipswich then went ahead from their first effort on goal after 17 minutes when Norris drilled the ball home after Gareth McAuley had headed a Jimmy Bullard corner back across the penalty area.
Norris's second goal of the season against the Clarets appeared to puncture Burnley's early optimism and within two minutes the visitors almost doubled their lead.
Andre Bikey, lining up in a new-look back four alongside debutant Shane Duffy and Brian Easton at left-back, was unlucky to be penalised for a challenge on Josh Carson.
But Bullard showed no sympathy as he whipped in a dangerous free-kick which Jason Scotland steered just over the bar from inside the six-yard box.
Shane Duffy impresses on debut
The Clarets offered little in response going forward and mid-way through the first-half went 2-0 down as Ipswich strolled to a second goal.
Scotland was left on-side from Norris's clever dummy and when he played the ball wide for Norris, the Town skipper crossed for Wickham to head the ball down and, with a bit of good fortune, up off the turf and over Lee Grant.
Howe didn't wait until half-time to try and change things as he sent on Chris Iwelumo in place of Wallace, who had just picked up a yellow card, to beef up a lightweight attack.
But the Clarets struggled to find any fluency and in an increasingly fractious game referee Trevor Kettle took his tally of bookings to five before the break.
Howe doubtless had words during the interval and the Clarets finally found a head of steam at the start of the second half as they took the fight to the Tractor Boys.
An Easton cross was headed down by Iwelumo for Marney to connect with a volley which Arran Lee-Barrett held at full stretch.
Captain Dean Marney tries to inspire a comeback
And when Easton crossed again, Eagles followed up to fire a in a low shot which was blocked in front of goal.
Suddenly the Clarets sensed a possible route back into the game and when Iwelumo released Nathan Delfouneso, the on-loan Aston Villa man did well to get an angled drive on target for Lee-Barrett to save.
Burnley needed to score, though, and just when it looked as though the momentum might be ebbing away Rodriguez struck with 68 minutes gone.
Wade Elliott had made an instant impression after coming off the bench and he was involved in keeping the ball alive for Marney to pick out Rodriguez to take a touch and then bury a stinging right-footed drive into the bottom corner from 22 yards.
Jay Rodriguez gives the Clarets hope
Ipswich hit back with Norris forcing Grant to touch his shot over the bar but Elliott then delivered a free-kick which the lively Defouneso poked just wide at the near post as the Clarets pressed for a leveller.
Elliott provided a constant threat as he staked a claim for a return to starting duty next weekend.
But when the winger's injury-time corner bobbled around the Ipswich box without a Burnley player being able to provide the decisive touch, time ran out on the comeback and another chance to bridge the three-point gap on the top six.
Burnley: Grant, Mears, Easton, Bikey, Duffy, Marney, Bartley (Alexander 75), Eagles (Elliott 67), Rodriguez, Delfouneso, Wallace (Iwelumo 36). Subs: Carlisle, Duff, Edgar, Jensen.
Booked: Wallace 30, Bikey 45, Delfouneso 78
Ipswich: Lee-Barrett, Edwards, Kennedy, McCauley, Delaney, Leadbitter, Carson (Dyer 79), Norris, Bullard, Wickham, Scotland (Drury 74). Substitutes: Peters, Healy, Civelli, O'Dea, Fulop.
Booked: Wickham 41, McAuley 42, Norris 45, Lee-Barrett 57
Referee: Trevor Kettle.