The council is now under no overall control after the Tories failed to secure an overall majority for the first time since 1976.
The new council is now made up of 22 Conservatives (-8 seats), 15 Independents (+3), 10 Lib Dems (+3), four Labour (+1) and one Green (+1).
Former council leader Ryan Fuller was the highest-profile Tory casualty, losing his seat to Independent Julie Kerr.
ITV News Anglia reporter Matthew Hudson was at the count on Friday, where he said the result was a "complete political shock" for The Conservative Party.
The constituency's Conservative MP Jonathan Djanogly admitted it had been a difficult day for his party.
"[It is] extremely disappointing, not least because I would maintain that the local Conservative administration has provided excellent services at a very low cost," he said.
"They didn't just manage Covid, they actually led on Covid, and we had a fantastic response and it's really sad to see that hasn't been recognised."
But there were celebrations too, among the other parties. Huntingdonshire has been a Conservative stronghold for decades, and the shift power has been hailed as a coup for other parties.
Ms Kerr, who secured 423 votes to Mr Fuller's 397 in the St Ives West ward, said local issues had been the key to her win against the former council leader.
"My biggest thing was asking them what they needed in time and looking to find out what their problems were and what their issues were.
"It was things like traffic. They found out from my leaflets that I was involved in the flood action group in St Ives off the back of the 2020 Christmas flooding so it just recognising that I care about people and talking about the things that concern them."
The council will not be dominated by one party as before, with there being no overall control.
The term refers to a situation in which no single political group achieves a majority of seats.
The council also has its first-ever Green Party councillor in Lara Davenport.
She told ITV News Anglia: "I think Green councillors are a different type of councillor.
"People see them on the ground in their communities, knocking on their doors, talking to them and knowing what the things are they care about and they want that personal touch from their councillor, and you've seen the response in the ballots today."
There are now expected to be negotiations between the parties and the Independents over the coming days before a new administration emerges.