Sylvan Ebanks-Blake appeared to have earned Wolves a well-deserved win when he struck for the 23rd time this season with a 73rd-minute strike.
But battling Ipswich were not to be denied although Miller could not have left his strike much later.
It was in the final few seconds of three minutes of stoppage time that Gary Breen was adjudged to have fouled Alan Lee 20 yards from goal.
Miller confidently strode forward to curl his shot over the wall and beyond the stranded Wolves goalkeeper Wayne Hennessey.
It was a rare moment of delight on the road for Ipswich Town who have won just three times away from home this season.
But for Wolves, Miller's strike could well have delivered a fatal blow to their promotion hopes.
A combination of poor finishing and smart goalkeeping ensured that the deadlock was not broken in an enthralling first half.
Wolves striker Andy Keogh wastefully fired over the bar after good work by Kevin Foley and Matt Jarvis before Ebanks-Blake squandered the best chance of the opening period for Mick McCarthy's team.
He was just two yards out when he met a 21st-minute cross from George Elokobi only to lift his shot over the bar.
It threatened to be a costly miss as Ipswich enjoyed a purple patch after his glaring error.
Jonathan Walters whipped in a vicious low shot on the turn in the 32nd minute that Hennessey did well to gather at his near post.
Hennessey then tipped away an Alan Quinn drive before frustrating Pablo Counago as Ipswich made a strong bid to take control of affairs.
But Keogh should then really have handed Wolves the initiative on the stroke of half-time only to head wide when well-placed after being picked out by Jarvis' corner.
After a first half of so many chances it was perhaps no surprise that the second period took some time to get going. When it did, Wolves emerged from a 60-second spell of pressure with the advantage.
Ebanks-Blake saw his header beaten away by goalkeeper Stephen Bywater and then had a follow-up shot inadvertently blocked on the line by team-mate Neill Collins.
But the former Plymouth marksman was not to be denied as seconds later he rifled home a 20-yard shot past Bywater.
It looked to be a match-winning strike only for Wolves to be denied by Miller's late, late show.