Thousands of people were affected at major airports including Glasgow, Edinburgh, Aberdeen, Prestwick, Heathrow, Stansted and Gatwick.
The National Air Traffic Service (Nats), said the issue, related to an internal telephone system, arose at its control centre in Swanwick, Hampshire, in the early hours of the morning when the night-time operation failed to properly switch over to the daytime system.
A Nats spokeswoman said: "At night, when it's quiet, sectors of airspace are combined. As it gets busier in the daytime, the sectors are split out again and additional control positions are opened to meet the traffic demand.
"Because of the problem with the internal telephone system, it was not possible to open the additional control positions this morning, resulting in a significant reduction in capacity in some areas of UK en-route airspace.
"Safety has not been compromised at any time."
By midday on a Saturday, Nats would usually have handled around 2000 flights. Yesterday that figure stood at 1700.
By yesterday evening the fault had been rectified and efforts were being made to clear the backlog.
Glasgow Airport tweeted: "A technical issue with air traffic control is resulting in some flight delays. Please check with your airline for specific flight info."
Edinburgh Airport said there were delays and cancellations and also advised passengers to check with airlines. Some flights were also reported to be delayed out of Aberdeen and Prestwick airports.
At Heathrow, the UK's busiest airport, there were 180 cancellations, split equally between arrivals and departures. A spokeswoman said: "We have around 25 minutes of arriving delays and 45 minutes of departing delays."
Many passengers took to Twitter to express their frustration.
Maeve Keegan, who was flying from Dublin to London, was delayed by two-and-a-half hours. But she also wrote on Twitter: "A couple on honeymoon missed connecting flight to Cancun! Nightmare."
Paralympic sailor Helena Lucas wrote: "Lots of angry people at Heathrow! Customer services is crowded with unhappy people! My flight looks on time fingers crossed!"
Take That singer Howard Donald tweeted: "Control tower failure at Heathrow has left me stranded for 2-3 hours at Dusseldorf, Anyone know any games besides eye spy?"
Other airports experiencing problems included Dublin, Cardiff, Luton, Newcastle, Bournemouth, Manchester and Liverpool.
Independent aviation analyst Chris Yates said: "It's going to be a day of frustrations, and the knock-on effects are going to last for the whole day because of the backlog of planes."
The Association of British Travel Agents said: "Customers due to travel should liaise with their airline to establish if there are any changes to their flight arrangements.
"Customers should be prepared for potential delays."