The National Air Traffic Service said the glitch happened at its control centre at Swanwick and required the service to limit the number of aircraft flying to ensure safety.
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Flights are beginning to restart from UK airports after a technical issue grounded and diverted planes earlier on Wednesday before engineers were able to restore the system, the air traffic control operator said.
Airports said it would take time for disruption to clear, with many planes and crew out of position.
The National Air Traffic Service (NATS) said the glitch happened at its control centre at Swanwick, southwest of London, and required the service to limit the number of aircraft flying to ensure safety.
London's Gatwick Airport said the issue affected outbound flights across the UK.
Some inbound flights were put into holding patterns or diverted.
Stansted, another London-area airport, said "many departures and arrivals" were affected and advised passengers to check with their airlines.
About 20 minutes after issuing an initial alert, the agency said engineers had fixed the problem and that it was "in the process of restoring normal operations."
Transport Secretary Heidi Alexander said "I am aware of a technical issue which impacted NATS’ operations causing travel disruption this afternoon."
"I have been informed systems have now been restored but continued disruption is expected, and passengers should check with individual airports for advice," she said.
The NATS system has suffered several software-related failures since it opened in 2002.
In August 2023, a glitch meant flight plans had to be processed manually, rather than automatically.
Hundreds of flights were delayed or cancelled at the height of the summer holidays and some 700,000 passengers affected.