The agency had identified a problem with the Notice to Air Missions system (NOTAM), which provides information to flight crews about hazards, changes to airport facilities and other essential information.
The system is used by pilots before they take off, meaning that there was no risk to flights that had left before the outage, the FAA said.
Airlines and airports had been left scrambling with news of the nationwide pause, as the White House said there was no immediate evidence of a cyberattack.
Near 1430 GMT, a screen at Reagan National Airport was overwhelmingly red with flight delays and just a handful of departures.
"Customers may continue to see some delays and cancellations as we work to restore our schedule," United Airlines said shortly after the FAA stop order was lifted, adding it would refund customers who no longer wish to travel.
Speaking to reporters, President Joe Biden said that he had been briefed by the transportation secretary and that "aircraft can still land safely, just not take off right now."
"They don't know what the cause of it is, they expect in a couple of hours they'll have a good sense of what caused it and will respond at that time," Biden said.
Transportation Secretary Pete Buttigieg directed "an after-action process to determine root causes and recommend next steps," he said on Twitter.
Senator Maria Cantwell, the Democratic Chair of the Senate Commerce Committee, also plans follow up.
"The number one priority is safety," Cantwell said. "As the Committee prepares for FAA reauthorization legislation, we will be looking into what caused this outage and how redundancy plays a role in preventing future outages. The public needs a resilient air transportation system."
Thousands of delayed flights
The NOTAM system is checked by pilots before they fly, the FAA said.
"A Notice to Air Missions alerts pilots about closed runways, equipment outages, and other potential hazards along a flight route or at a location that could affect the flight," the agency tweeted earlier Wednesday.
The FAA had halted flights until 9:00 am (1400 GMT), but began resuming takeoffs at Newark and Atlanta airports before the nationwide order was lifted due to air traffic congestion.
White House Press Secretary Karine Jean-Pierre tweeted that "there is no evidence of a cyberattack at this point."
"The President directed DOT to conduct a full investigation into the causes. The FAA will provide regular updates," she said, referring to the Department of Transportation.
There were more than 5,400 flights delayed in the United States by 10:00 am US Eastern time (1500 GMT), flight tracking website Flight Aware data showed.
The halt comes in the wake of a large-scale aviation meltdown in the United States over the Christmas holiday, as a storm brought unseasonably cold temperatures to the majority of the country and caused chaos, with thousands of flights delayed or canceled.
Hard-hit Southwest Airlines canceled more than 15,000 flights over eight days after what it said was a breakdown in its scheduling systems.