Brian Barry-Murphy’s young side created several excellent chances while Brazilian teenage forward Kayky came on as a second half substitute to make his club debut.
But five second half goals ensured the spoils went to the Millers, for whom Kieran Sadlier struck a hat-trick, as they made it three wins out of three in Group E
City’s faint hopes of a possible second place finish now rest on the outcome of the final group match between Scunthorpe and Doncaster next month.
With Rotherham flying high in League One and having won both their opening Papa John’s group games it promised to be another tough examination for Brian Barry-Murphy’s side.
It proved a cagey opening at the AessealNewYork Stadium with both sides pressing high and probing at every opportunity for an opening.
A searing run from James McAtee on 11 minutes saw the midfielder then tee up Micah Hamilton cutting in from the left but the City winger’s shot was comfortably saved by Millers keeper Viktor Johansson.
The hosts then warmed Cieran Slicker’s hands in the City goal with Freddie Ladapo letting fly from 20 yards.
A wonderful searching ball from Romeo Lavia forced Johannson to race out of his box to just deny the advancing McAtee with the keeper requiring lengthy treatment for his bravery.
Another sublime long range Lavia pass again found McAtee, time raiding down the right, and from the midfielder’s square ball, Liam Delap fired in on goal but his effort was too high.
Some superb strength from Delap in the Rotherham box then teed up Shea Charles and it took a fine save from Johannson to deflect his shot over the bar.
More magic footwork from Wilson-Esbrand then almost unlocked the Rotherham defence before a deflected Delap shot whistled wide.
City made a double switch at the break with Brazilian teenage forward Kayky coming on for his Club debut with Nico O’Reilly also called into action.
And City almost made an instant second half breakthrough with only a smart Johansson save denying McAtee.
However, it was Rotherham who made the all-important breakthrough on 51 minutes. After Mbete’s ball out had been intercepted, substitute Will Grigg deflected Kieran Sadlier’s 18-yard drive past Slicker into the net.
City could have drawn level almost immediately. Bobb worked wonders to win the ball back on the edge of the box and then put in McAtee behind the Millers defence.
His cross found Kayky unmarked at the edge of the right box but the 18-year-old’s shot was just too strong.
City stormed forward once more with Johansson again denying McAtee before O’Reilly’s follow up shot was deflected over.
It was now end-to-end stuff with Slicker then alert to deny Sadlier in a one on one after Rotherham had wrested possession on the halfway line.
But City’s task was made all the tougher on 63 minutes as the hosts doubled their lead from the penalty spot.
Finley Burns was adjudged by referee Samuel Barrott to have brought down Kayode in the box and Sadlier sent Slicker the wrong way from the resulting spot kick.
And with their tails up, Rotherham extended their lead on 67 minutes as Jake Hull found a pocket of space to guide Mickel Miller’s corner past Slicker and all but seal a third straight group victory.
O’Reilly and Lewis came agonisingly close again before Sadler then added his second and Rotherham’s fourth goal nine minutes from time.
And a disappointing second half was sealed when Sadler completed his hat-trick with a 90th minute free-kick
How we lined up
Cieran Slicker was in goal shielded by a back four of Rico Lewis, Luke Mbete, Finley Burns and Josh Wilson-Esbrand. Romeo Lavia was the holding midfielder with Shea Charles and James McAtee also in the engine room. Oscar Bobb, Liam Delap and Micah Hamilton were the forward trio.
What it means
While Rotherham are assured of their place in the knockout stages, City must now wait for the outcome of the final group game between Scunthorpe and Doncaster.
Like City Doncaster have three points but City boast a marginally better goal difference while Scunthorpe are without a point.
They meet on November 9th to determine who will finish second in the group and so go through to the round of 32.
Brian Barry-Murphy’s side are back in action on Friday when we resume PL2 action away at Brighton Hove Albion.
Kick-off on the South coast is at 7pm and CITY+ subscribers will be able to watch all the action live on our app and website.
News about Rotherham v Man City
Ticket information: Rotherham v City EDS
Papa John’s Trophy - Ticket Information Read more
EDS aim to heed lessons from Papa John's Trophy, says Barry-Murphy
Brian Barry-Murphy says the short term pain of Tuesday’s Papa John’s Trophy loss at Rotherham for City’s Elite Development Squad can give way for the long term gain of the overall learnings from the competiton. Read more
Highlights: Rotherham 5-0 City EDS
City’s Papa John’s Trophy group campaign ended on a disappointing note as our Elite Development Squad lost out at Rotherham. Watch more
Full Match Replay: Rotherham v City EDS
Watch the entire 90-minutes of Manchester City Elite Development Squad's trip to Rotherham United. Watch more