The unbeaten League One leaders toiled for 92 minutes against Gary Naismith's men but were handed their breakthrough deep into time added on when substitute Stephen O'Neill hacked down David Templeton.
That gave skipper McCulloch the chance to role home from the spot and he made no mistake as he took the Ibrox side to within two wins of the title and promotion to the Championship.
The build-up to the match was overshadowed by the ongoing rows between former director Dave King and the Light Blues board.
And there was a sense that McCoist's men were distracted as they failed to cut through the determined Fifers.
Rangers boss Ally McCoist made two changes to his side as David Templeton and Dean Shiels returned to the starting line-up, with Steven Smith and Arnold Peralta dropping to the bench after failing to impress against Stranraer in midweek.
Naismith, meanwhile, was able to welcome another Ibrox old boy Steven Hughes back into his side after his short-lived move to Dundee.
After a tentative start, the champions-elect came within an inch of a 12th-minute opener when Templeton threaded a pass in behind the Fifers' defence before Dean Shiels poked just wide.
But Rangers have not impressed for most of the past two months and their carelessness was evident again soon.
Ricky Foster was well placed to hack away Gary Fisher's volley on the quarter-hour, but moments later the right-back's poor headed clearance allowed the same player to slam the ball into the side-netting as the home side came close again.
That was as long Fisher lasted, though, with the former Kilmarnock midfielder forced to trudge off with a shoulder injury after colliding with Ian Black to be replaced by O'Neill.
There had been plenty of angry words written in the numerous statements released throughout the week as the Ibrox power struggle rumbled on.
But there was little aggression in Rangers' play in the first half an hour as they seemed happy to pass the ball with out the threat of a final ball.
When they did go up a gear, Greg Paterson's right-hand post denied Nicky Law after Lee Wallace's deflected shot broke for the Englishman while Templeton was denied by the keeper after driving in from the right.
By the time McCoist's side had returned for the second half, though, they had reverted to training mode as they laboured.
It took until the 58th minute for them to mount a serious attack but even then defender Joe Mbu did well to cut out Fraser Aird's dangerous low cross to the front post.
Templeton dragged a hopeful effort wide on 70 minutes but there was little to lift the spirits of the travelling Rangers support after another weary few days.
They did better with 10 minutes left as Templeton robbed Kevin Rutkiewicz before driving through to fire off a shot from a tight angle, but Paterson pushed the strike away.
McCulloch was presented with a decent chance as he peeled away to the back post at a Wallace free-kick but could only aim a knee at Jon Daly's knock down, allowing Paterson to gather.
Templeton then did well to work space on the edge of the box but again Paterson came up with a save as he sprang to his left to deny the winger's strike.
But the former Hearts man kept trying and in stoppage time his trickery fooled O'Neill into a silly challenge and referee Alan Muir and the was immediate as he pointed to the spot.
McCulloch took responsibility and the captain eventually gave his team's faithful some cheer as he sent Paterson the wrong way to clinch Rangers' 25th win of the league campaign from 27 games.