Played in front of a crowd of 31,213 - smashing the Women's Super League record - City recovered from a laboured first-half display to start the new campaign with a historic win.
Caroline Weir's 25-yard stunner was the difference, a thumping effort into the top corner that gave Mary Earps in the United goal no chance.
The first big chance fell to United. Former City striker Jane Ross was picked out by a ball in from the left, but her first-time effort from five yards out was superbly saved by Ellie Roebuck, the City ‘keeper somehow clawing the ball away as it headed for the top corner.
It was a moment of brilliance from Roebuck that maintained parity, despite City being off the pace in the opening stages.
We were struggling to create clear-cut chances, but a fine move started by Keira Walsh, so often the creative spark in Cushing’s side, ended with Weir forcing Mary Earps into a decent save with a powerful effort from distance.
That seemed to lift City. Moments later, United failed to deal with Georgia Stanway’s free-kick and the ball fell to Janine Beckie at the back post, but she opted to try and finish with her right when the left seemed a better option and she failed to turn the ball home. It was a big opportunity missed.
City, though, were finally finding some rhythm.
The second half started superbly for the home side. A loose ball out from the back was intercepted by Weir, who drove forward and unleashed a remarkable left-footed effort that flew into the top corner from 25 yards. It was a moment of outstanding quality befitting of such a grand occasion.
City were suddenly enjoying themselves, and a swift counter from a United corner ended saw Beckie sprint almost the full length of the pitch before blasting an effort just over the bar.
United almost levelled late on when Jackie Groenen’s deflected effort rolled past Roebuck - but the ball hit the upright and the City stopper claimed it.
Relief and huge cheers greeted the full-time whistle. This wasn't vintage City. It was a momentous and testing occasion but we found a way to win.
Player of the Match: Caroline Weir
A constant menace and a wonderful goal. She won't forget this match in a hurry.
Special mentions, too, for Beckie, who was dangerous throughout, and Roebuck, whose first-half save was crucial.
What it means
City have opened the new WSL season with three points, the perfect start for a side with aspirations of regaining the trophy we last won in 2016.
But perhaps more significantly is the gravitas of the win. The first-ever women’s Manchester Derby, played in front of more than 30,000 at the Etihad Stadium, had a seismic feel to it.
City’s players have ensured they will forever be remembered by fans and record books alike.
City travel to Switzerland this week to face Lugano in the Champions League, before next Sunday’s WSL trip to Reading.
The season has started and the games immediately come at a relentless pace, but Cushing, who added seven new players over the summer, has assembled a top-class squad capable of withstanding the demands of competing on four fronts.
A good start is vital, and the squad will be buoyed by their historic victory today over local rivals Manchester United.
News about Man City v Man United"
Classic highlights: City 1-0 United
Ahead of Sunday's FA Cup clash with Manchester United, take a look back at the Derby which started it all... Watch more