The bookies predict their combined loss will be around $21m but if all the initial Leicester backers held on to their tickets, the losses would have been closer to $75m.
There are great punting stories from both ends of the scale.
A Guildford man placed $160 on Leicester a few weeks into the season, when bookies had already reacted to the Foxes' strong start and slashed their odds to 1500 - 1. If Leicester win the EPL he will scoop $240,000 which is the largest ever win on the EPL.
The BBC reports that "the world's most calamitous punter" put $1 on Leicester to win at 5000 - 1, and made an immediate loss by cashing out after opening day for 90 cents. If Leicester wins the EPL, he will miss out on $5000.
Ladbrokes spokesman David Williams said: "It is an absolute mystery. He must be feeling pretty sick. He must have thought the wheels were going to come off after the first win and decided to cut his losses."
Ladbrokes want to offer him a consolation prize to "soften the blow", as early as this weekend. Leicester will automatically win the title if they beat Manchester United or Tottenham Hotspur lose to Chelsea.