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Ronnie Moore's Millmoor outfit deserved the win over their high-flying neighbours but squandered a string of second-half chances.
United keeper Paddy Kenny pulled of brilliant fingertip to deny Rotherham a first-half lead.
Michael Proctor swivelled and shot on the turn with a rising effort and looked set to put Rotherham ahead, but the Irish keeper stretched to turn it over.
United had been second best and hardly deserved to be level at the break, but could have been in front as early as the tenth minute.
Dutchman Dries Bousatta opted for a spectacular volley when he had time and space and blazed over United's best effort.
Rotherham carved out the lion's share of the chances, but failed to cash in. Among the guilty was Paul Warne who blasted over from 18 yards.
Monkhouse was denied by a Kenny save, Martin Butler scuffed a shot and John Mullen fired wide.
But just a minute into the second half United went ahead through Jack Lester's 13th goal of the season.
Striker Andy Gray twisted and turned in the area and coaxed Chris Swailes into a rash challenge, earning the spot-kick that Lester tucked away with a cool finish.
But four minutes later the home side were level. Butler broke down the right cut inside and pulled back an inviting pass for Monkhouse to clip home his third goal in the last four home matches.
Rotherham continued to make the running, but squandered a string of chances that should have earned them the win.
Butler was twice off target with a pair of headers before a Proctor shot was wasted.
Kenny again saved United with a reaction stop to turn away Butler's 76th minute shot and Warne blazed wide after Scott Minto's cross.
But in the dying seconds Mike Pollitt produced his a splendid save to deny Michael Tonge, blocking a blistering drive.