The goal came after 73 minutes, though Miller might have scored after 25 seconds but for a Fabian Wilnis block.
Darren Anderton later forced a save from Ipswich keeper Shane Supple.
Dean McDonald almost converted a cross for Ipswich, while Darren Currie curled a shot just wide and Stefan Postma saved from Scott Barron.
Ipswich manager Joe Royle:
"I can't dispute that it was a penalty.
"Our right-back has been outstanding for us but when he does make a mistake, there is a tendency for the ball to end up in the back of our net.
"And that was the only way I could see Wolves scoring - from a penalty, a corner or a free kick."
Wolverhampton: Postma, Ross, Lescott, Craddock (Edwards 38), Naylor, Davies, Rosa (Ricketts 89), Anderton, Miller, Cort, Frankowski (Aliadiere 60).
Subs Not Used: Oakes, Ganea.
Booked: Ross, Davies, Naylor.
Goals: Miller 74 pen.
Ipswich: Supple, Sito, Wilnis, De Vos, Barron (Proudlock 48), Currie, Garvan, Westlake, Richards, Naylor, McDonald (Peters 58), Peters (Magilton 75).
Subs Not Used: Brekke-Skard, Price.
Booked: Sito, Westlake, Magilton.
Ref: K Woolmer (Northamptonshire).