At the start of the season, the Foxes were given a 5,000-1 chance of finishing on top.
Leicester's own Gary Lineker said he could not think of anything in sporting history that could surpass the achievement.
But what does it mean to the rest of the city?
Hundreds of fans young and old gathered in front of the King Power stadium minutes after Tottenham's 2-2 draw at Chelsea on Monday night, confirming the team's place at the top of the Premier League.
Mark Smith, a lifelong Leicester fan, said he was one of the first at the Foxes ground: "It was just me and [Leicester East MP] Keith Vaz!
"I can't describe it it's unbelievable we have waited so long," he said.
"It does feel like a fairytale - the bookies must be kicking themselves."
Fans sang their hearts out amid blue flares, car horns and chants of "champ-i-ooons".
The Chauhan family were there too.
Dhara Chauhan said "Chelsea, you had one job and you did it - thank you!"
Even fans of other teams were were moved to join the party, which continued into the early hours.
"Just look at this, it's amazing there are mums and dads getting their kids up to see this. For it to come to this is unbelievable,"  said Liverpool fan Mark McGlinchey, who has lived in Leicester for 12 years.
And Arsenal supporter Ash Patel said: "This is madness, it's the most incredible thing I've ever seen."
Hundreds more spilled out of the pubs on to the city centre streets and around the clock tower, where there were drums beating, car horns blaring and unrelenting chanting well into Tuesday.
Nathan Battu said: "You look at everyone here chanting we are staying up. Everyone's surprised we stayed up never mind down the league!
"People crowded here on a whim really and look how many people there are."
In the sober light of day, Leicester City's achievement seems all the more incredible given how their chances were viewed at the start of the season.
Claudio Ranieri, whose famous "Dilly ding, dilly dong" phrase could be heard sung out throughout the night, was considered an uninspired choice by many and Leicester's outlook was bleak.
To put those 5,000-1 odds into context, there was more chance of Sir Alex Ferguson winning this year's Strictly Come Dancing.
Time to get your dancing shoes on, Fergie?
A "fairytale come true" is how Leicester's historic Premier League win against all the odds has been described by fans.