Sachindu Colombage took three wickets on his Sri Lanka debut as England were restricted to 265 all out in the first one-day international at Chester-le-Street on Tuesday.
The home side, despite a tricky pitch on which the ball was not coming onto the bat, were well placed for a large total at 182-3 in the 32nd over after captain Harry Brook won the toss.
But Sri Lanka then took three quick wickets to reduce England to 199-6.
Legspinner Colombage dismissed Joe Root and Jos Buttler during an impressive return of 3-44 in his full 10 overs, with Brook's 67 the only fifty of the innings.
But allrounder Will Jacks's unbeaten 46 off just 47 balls, featuring four consecutive fours off Dushmantha Chameera, bolstered England's total.
England, however, failed to bat out their full 50 overs, with 11 balls remaining when last man Josh Tongue was expertly yorked for a duck by paceman Asitha Fernando (3-53) to end the innings.
England, who crushed Sri Lanka 3-0 in their T20 series earlier this month, lost Tom Banton early, bowled by a superb Fernando delivery that clipped the top of off stump.
And when fellow opener Ben Duckett was lbw for 32, trying to sweep left-arm spinner Dunith Wellalage, England were 67-2.
Test skipper Root and Brook rebuilt the innings with a third-wicket partnership of 68.
Root, however, was eventually dismissed for the first time in five ODI innings – a sequence spanning 404 runs – when he was bowled playing back for 44 to a fine delivery from Colombage.
But Brook continued his fine form from the T20 series with a 49-ball fifty including six fours.
Brook carved seamer Chameera straight to deep cover before Colombage had the dangerous Buttler (31) lbw on review as England lost momentum.
And they were 199-6 when Rehan Ahmed, in for the injured Adil Rashid, carelessly strolled out of his crease only to be run out by Charith Asalanka's direct hit from cover.
The second game of the three-match series takes place at Headingley on Thursday.