The summer signing from Shamrock Rovers suffered an injury shortly after his switch but proved well worth the wait as he grabbed a goal and an assist in a topsy-turvy South Yorkshire derby.
Anything more than a point for Rovers would have taken them into the knockout stages along with Manchester United U21s.
But now any one of Rotherham, Doncaster or Lincoln City can make it through the group with the Old Trafford youngsters.
Rotherham led early at the New York Stadium when Rovers' skipper-for-the-night Joe Wright headed into his own goal.
But Wright atoned for his error - after Kieran Sadlier equalised with a stunning strike before the break - by sending home a fine header at the right end.
The Millers levelled with a fine finish from Carlton Morris, laid on by Clarke who then won a penalty which Morris missed.
But the Miller did go ahead again on 76 minutes when Clarke surged through and slammed past Lawlor.
The frantic tipping of the balance of the game could hardly have been predicted by a flat opening period - punctuated only by the goals of Wright and Sadlier - in front of a sparse crowd at the New York.
Demonstrating where the competition fits in the two sides' priority lists, both rang the changes - the Millers made eight, Rovers nine.
It meant much of the evening's interest centred on the new faces.
Julien Lamy made his long-awaited first start for the Millers and impressed with lively footwork and plenty of confidence.
And for Rovers there was a first glimpse of new signing Kwame Thomas, operating as the lone striker in Darren Moore's 4-2-3-1 system. He initially lost out in the physical battle with the Rotherham defence but then produced a couple of excellent flick-ons - one of which led to Sadlier's equaliser.
But the headlines would go to Clarke, who kicked off his Rotherham career with a real bang after coming off the bench at the break.
Prior to his introduction, Clarke will have watched his side enjoy the better of the opening half as the Millers made their greater experience on the night count.
The hosts had the better cohesion and greater tempo as Rovers struggled to get going and maintain any possession of their own.
The deadlock was broken on 11 minutes when Billy Jones sent in a wonderful cross, forcing Wright to act but his attempt at a blocking diving header only sent the ball cannoning past Ian Lawlor.
It took Rovers a while to recover and Lawlor was forced into a smart save from Freddie Ladapo before Morris headed straight at him moments later.
Thomas offered the first element of threat for Rovers when he met a cross from Alex Kiwomya with a stooping header but sent it well over the bar.
And the new signing showed exactly what he can add to Rovers with his part in the equaliser.
Thomas rose well to flick on a long clearance and send Sadlier racing away before he smashed an unstoppable effort beyond Lewis Price from the corner of the box.
Rotherham recovered with Ben Wiles testing Lawlor from distance while the lively Lamy rattled the bar with a strike from 30 yards.
But within nine minutes of the restart Rovers were ahead. Alfie May clipped in a cross and Wright dipped away from his marker before looping a header into the corner. The Rotherham coaching staff were furious as they waited to send on a replacement for the injured Shaun MacDonald.
Morris missed a glorious chance to level immediately when sending a header straight at Lawlor from point blank range.
But it was his turn for atonement on 67 minutes when he latched onto Clarke’s stunning through ball and slammed past the Rovers keeper.
Four minutes later Rotherham won a penalty when Clarke was tripped by a combination of Wright and Donervon Daniels but Morris’ effort was tame and easy for Lawlor to keep out.
Clarke ensured the miss was not rued for too long as he grabbed the winner 14 minutes from time. Morris sent him through and he finished confidently into the far corner.
ROTHERHAM: Price; Jones, Cooper, Robertson, Mattock; MacDonald (Lindsay 55); Morris, Wiles, Barlaser (Kayode 73), Lamy; Ladapo (Clarke 46). Subs not used: Bilboe, Ihiekwe, Olosunde, Hinds.
ROVERS: Lawlor; Halliday (Daniels 46). Wright, Blaney, Amos; Greaves, Gomes; Longbottom, Sadlier (May 46), Kiwomya; Thomas (Taylor 76). Subs: Dieng, James, Sheaf, Watson.
REFEREE: Marc Edwards
ATT: 2,191 (557 away)