The victory was particularly contributed by Azmatullah Omarzai who seized a five-wicket haul. In the penultimate over, Fazalhaq Farooqi had claimed Jofra Archer to make it 13 runs required for England with just one wicket in hand.
Omarzai saw the game through by claiming Adil Rashid in the final over. He had removed Joe Root and Craig Overton as the game went down to the wire.
Root scored his ODI century bringing to an end a long wait for a hundred in the 50-overs game.
The England batting talisman s resolute innings came against wickets falling at regular intervals at the other end as he held the fort from one end and took the attack to the Afghan bowlers.
Compiling 120 off 111 deliveries, Root laced his innings with 11 fours and a six, playing the anchor for England.
Defending the total, Afghanistan were off to a steamy start with the all-round duo of Omarzai Mohammad Nabi striking in the powerplay.
Omarzai skidded one through Phil Salt to hit the timber. Mohammad Nabi also got the better of Jamie Smith off the first ball of his spell to make it two wickets for Afghanistan.
Root then combined alongside Ben Duckett to add 68 runs for the third wicket but just as the pair seemed to be putting together a game-changing partnership, Rashid Khan struck with the ball.
Earlier, Afghanistan skipper Hashmatullah Shahidi won the toss and have opted to bat first.
Ibrahim Zadran forged 177 runs off 146 deliveries, lacing 12 fours and six maximums as Afghanistan put on their highest-ever total in ICC Men s ODI tournaments.
With three wickets down at the end of the powerplay, Zadran combined alongside skipper Hashmatullah Shahidi to add 103 runs for the fourth wicket as Afghanistan turned the tide.
Shahidi was removed by Adil Rashid in the 30th over but Ibrahim kept the scoreboard ticking, becoming the first-ever Afghanistan batter to score a hundred in the ICC Champions Trophy.
For England, Jofra Archer had ripped into the Afghanistan top-order in his news ball burst. The tearaway quick had nipped one into the right hander who played it onto his stumps. The right-arm quick then trapped Sediqullah Atal leg before wicket in the same over to reduce the Afghans to 15/2.
Afghanistan: Rahmanullah Gurbaz, Ibrahim Zadran, Sediqullah Atal, Rahmat Shah, Hashmatullah Shahidi(c), Azmatullah Omarzai, Mohammad Nabi, Gulbadin Naib, Rashid Khan, Noor Ahmad, Fazalhaq Farooqi
England: Phil Salt, Ben Duckett, Jamie Smith, Joe Root, Harry Brook, Jos Buttler(c), Liam Livingstone, Jofra Archer, Jamie Overton, Adil Rashid, Mark Wood
