The 22-year-old City star won the free-kick that Marcus Rashford opened the scoring from before adding a quickfire second a minute later.
It was a memorable night for City’s England quintet, who all all featured, with Foden, Kalvin Phillips and Kyle Walker all making their first appearance in Qatar.
Walker, sidelined since September after surgery, looked sharp from the kick-off, sustaining one heavy challenge without any issues and using his pace down the right flank to great effect.
John Stones was his usual calm and collected self in central defence, though the Welsh barely left their own half as the Three Lions dominated possession.
However, the teams went in goalless at half-time
The in-demand Foden, making his first appearance at a World Cup tournament, had been lively throughout the opening 45, always trying to up the pace and find ways through a disciplined Wales defence.
But, though the City playmaker toiled without reward in that first period, he made an immediate and devastating impact just after the break.
It was Foden’s mazy run that ended with him being felled just outside the Wales box and Marcus Rashford’s sweetly-struck free-kick put the Three Lions 1-0 up.
And a minute later, Foden showed why much of the nation had been clamouring for his inclusion in the starting XI as he doubled England’s lead, turning in Harry Kane’s precise low cross at the far post to double the advantage.
On 57 minutes there was also the welcome sight of Kalvin Phillips entering the fray as he replaced Declan Rice on what was proving a wonderful night for City players.
During what was a triple substitution, Walker’s successful return to action ended as he was replaced by Trent Alexander-Arnold.
And Phillips took just 11 minutes to show his international pedigree as his clever lofted ball set Rashford away on the right flank and the Manchester United man cut inside the Wales box before drilling home his second and England’s third.
Jack Grealish ensured the full contingent of City players had taken part when he appeared as a sub for Rashford on 76 minutes.
In added time, Stones went agonisingly close to scoring as he poked Harry Maguire’s headed cross over the bar from six yards.
There was no further scoring with England taking their place in the Round of 16 where they will face Senegal on Sunday for a place in the quarter-finals.
