The technical glitch, at an air traffic centre in Leesburg, Virginia, caused delays of nearly three hours in some cases.
A spokesperson for the Federal Aviation Administration (FAA) said later that it had resolved the issue.
Planes would be able to take off normally by about 16:00 EDT, the FAA said.
The affected airports are among the busiest in the United States, especially in the summer holiday months.
Among those hit by the glitch were Washington’s Dulles International Airport and Reagan National Airport, as well as New York’s LaGuardia and JFK International Airport.
The FAA said the problem is not believed to be caused by any accident or hacking.
According to the agency, the fault was with a computer system known as ERAM which is used at 20 air traffic control centers around the US that handle high-altitude air traffic.
The system was installed earlier this year but was already years behind schedule.
“The FAA is continuing its root cause analysis to determine what caused the problem and is working closely with the airlines to minimize impacts to travelers,” the agency said in a statement.
Flight tracking service FlightAware reported that about 400 flights had been delayed or cancelled across affected airports.
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