And Jack Grealish made it five Blues in white with a cameo off the bench with five minutes or so remaining as the Three Lions booked a place at next summer’s European Championships in Germany.
Four of City’s quintet of England players were named in the starting XI.
In a disjointed start, there was little to report in the way opportunities or flowing play, and it was Italy who opened the scoring on 16 minutes when Gianluca Scamacca slammed the ball high into the roof of the net from Giovanni Di Lorenzo low cross from the right.
Italy were causing problems by their willingness to put numbers in the England box whenever they attacked, but crucially, it would be the hosts who scored next.
Jude Bellingham raced onto a pass into the box, and he got to the ball a fraction before Di Lorenzo’s sliding challenge which brought the Real Madrid man down to the turf.
The referee pointed to the spot and after a lengthy VAR check, Harry Kane tucked away his 60th goal for England with consummate ease with 31 minutes on the clock.
Just four minutes after, the busy Di Lorenzo almost fashioned a second goal for the Azzurri with another overlapping run and dangerous cross that was expertly cut-out by Stones on this occasion.
Four minutes after the break, Foden went down in the box but no spot-kick was awarded on this occasion, and not long after, Foden laid the ball off for Phillips who sent a shot over the bar from 20 yards.
The Three Lions went ahead for the first time on 57 minutes when Marcus Rashford fired a low shot home after cutting in from the left after fine work from Bellingham.
Stones’ evening ended when he was substituted to warm applause on 63 minutes, with Southgate not wanting to push the City defender too hard in what his first start since the FA Community Shield at the start of August
Foden had the Wembley crowd on their feet with excitement as he weaved his way past his marker and into the box with a run full of vim and vigour, but Rashford couldn’t convert the cut-back he sent in.
Foden then exchanged passes with Bellingham on the edge of the box before seeing a low shot well saved by Donnarumma.
With Phillips on a yellow card – and having been a shade fortunate not to have received another for a borderline challenge – the Blues’ combative midfielder was replaced by Jordan Henderson on 69 after a steady, tidy performance.
Kane sealed victory with a fine solo goal on 77 minutes to make it 3-1 and ensure England qualify from Group C with two games to spare.
Grealish replaced man of the match Bellingham on 85 minutes but had little chance to affect proceedings on what was a hugely satisfying night for the Three Lions.
“We knew it was a massive game. I think the result epitomises what we are all about.
“With this England team we are always going to start well because we have such good players on the pitch but when we get a setback we have the driving force of Jude Bellingham and Harry Maguire and the trickiness of Marcus Rashford to come into the side.
“I scratch my head sometimes and wonder how is Jude getting better and better. He is very humble and very level headed. Marcus is the same.”