Hundreds of flights have been cancelled or delayed since Thursday, when authorities revealed an alleged plan to attack several trans-Atlantic flights with liquid explosives.
The situation has already cost all carriers millions of dollars a day, and budget airlines could be even more susceptible to future costs.
David Bryon, an industry consultant and former managing director of low-cost airline Bmibaby, said on Monday: "The situation as it is at the moment is unsustainable."
No-frills carriers are particularly vulnerable to increases in turnaround times - the interval between when a plane lands and when it takes off again with a new set of passengers.
Speedy turnarounds mean more flights and reflect the budget airlines' decision not to offer full onboard meals and to discourage passengers from checking bags - costly services that eat up time and staff on the ground.
Fast groundwork is the main way that the no-frills carriers keep down costs and fares.
Ryanair Holdings says it has a turnaround time of 25 minutes, while its major competitor EasyJet aims for just five minutes more.
But with passengers stuck in lengthy queues at airports around the country because of strict security checks, those numbers are currently far out of reach.
"The problem is that the budget airlines work to tight schedules," said Bryon.
"The UK government, by insisting on these heavy-handed security measures, is allowing the extremists to achieve many of their objectives"
Ryanair chief executive
"If you can't physically do that because of passenger checks, you can't meet your turnaround timetable, you have to consider changing your schedule and costs rise."
The government slightly eased strict security measures that had banned all carry-on baggage as the threat level was lowered on Monday.
The UK transport department said passengers would be allowed to carry a single, briefcase-sized bag aboard planes, and that books, laptop computers and digital music players would be permitted again.
But BAA, the operator of Heathrow and other major London airports that has struggled to deal with the chaos, said it would not adopt the relaxed regime until Tuesday.
It also ordered airlines to cut Monday's services by 20% or face the loss of all their flight slots, drawing complaints from airlines.
Nigel Turner, Bmibaby's chief executive, said the airline was following BAA's directive but he hoped the situation would have returned to "pretty much as normal" by the end of the day.
EasyJet, which has cancelled more than 500 flights since Thursday, continued to ask its passengers on Monday to pack everything into one piece of luggage for the hold in an attempt to minimise the volume of bags it has to deal with.
Meanwhile Ryanair, which has grounded a fifth of all scheduled departures since Thursday, was critical of both the BAA and the government.
"The UK government, by insisting on these heavy-handed security measures, is allowing the extremists to achieve many of their objectives," said Michael O'Leary, the company's chief executive said.