Former Rangers' striker Miller, who has signed a pre-contract agreement to join Celtic in the summer, struck from the spot in the 73rd minute after substitute Jeremie Aliadiere had been fouled by Sito Castro.
To say it was a rare penalty for Wolves is something of an understatement. It was the first they had been awarded since the spot-kick they won at Crewe in March last year and the first at Molineux since the game against Millwall in December 2004.
Wolves were full value for their success against an in-form Ipswich side who had arrived at Molineux level on points with Wolves after winning their previous three games.
Ipswich were pegged back for long spells, but did start the second half brightly and should really have made that golden spell pay-off before Miller sent them crashing to their first defeat since December.
Twice in the space of four minutes Ipswich midfielder Ian Westlake was in the clear only to be denied by Wolves' goalkeeper Stefan Postma and then shoot wide from six yards.
They were costly misses as Wolves cut the gap on sixth-placed Preston to five points with Ipswich still eight points away from the play-offs.
It was a major surprise that the game reached half-time goalless as both sides created a host of chances without producing the one piece of class that would have broken the deadlock.
Denes Rosa, Tomasz Frankowski, Darren Anderton, Jody Cradock and Mark Davies all squandered clear openings in the first 20 minutes for Wolves.
It was therefore ironic that the first goalkeeper to be seriously tested was Postma.
He did well to palm away a low 27th minute drive from Owen Garvan after being picked out by a neat pass by Matt Richards.
But it was Wolves who continued to look the most potent attacking force with Ipswich keeper Shane Supple doing well to hold a 30th minute header by Miller.
Supple denied the Scottish international again nine minutes later but was powerless to prevent him making the decisive contribution from the spot.