The visitors' secondary did a job on Philadelphia, who turned the ball over four times on Monday night after previously only giving up three turnovers in their unbeaten first eight games.
The Eagles went into halftime trailing for the first time this season, with home quarterback Jalen Hurts almost ensuring victory late in the fourth quarter.
While down 26-21, the Oklahoma-via-Alabama product connected on a 51-yard pass to Quez Watkins, but the wide receiver fumbled following the reception to hand Washington possession.
Taylor Heinicke, standing in for the man Hurts replaced at Lincoln Financial Field, Carson Wentz, was efficient as he went 17 for 29 and 229 yards through the air.
Washington's Terry McLaurin recorded 128 yards receiving, which included a 41-yarder that led to a field goal.
"We had a marvellous time ruining everything," the Commanders tweeted after snatching their fourth win in five games, taking their season to 5-5 and ensuring the Eagles moved to 8-1.