Charles Carter, 33, was filmed by an anti-hunt campaigner at a meeting of the North Yorkshire-based Middleton Hunt.
In the phone footage, the woman confronts Mr Carter - accusing the hunt of illegally chasing a fox.
Dressed in full red hunting attire and apparently filming the encounter himself on his phone, he tells the protester: "I'd quite like the shag you, actually."
After the woman responds "I'll tell my husband that then, shall I?", Mr Carter adds "can I take you to bed, please?", tells her she is "very pretty" and asks for her phone number.
Mr Carter was suspended from Breckland Council, in Norfolk, on Wednesday
At the time, the council said he has been suspended after it had "been made aware of a video of a hunt in Yorkshire in which one of its councillors, Charles Carter, made inappropriate and offensive comments to a protester".
Council leader William Nunn, said on Wednesday: "Having been made aware of the video this morning, I was appalled by the conduct of one of my Conservative Councillors who has clearly brought the party and the Council into disrepute as a result of his behaviour.
"I immediately took action and the individual concerned has been suspended from the Conservative Group at Breckland Council pending the outcome of a full investigation by the Mid Norfolk Conservative Association."
On Thursday, the council confirmed the councillor's resignation.
It said in a statement: "Cllr Charles Carter is to step down with immediate effect from his role as a Breckland Councillor for Saham Toney ward.
"On Wednesday (25 January) he was suspended from the Conservative Group at Breckland Council by Leader William Nunn, pending the outcome of a full investigation by the Mid Norfolk Conservative Association into concerns relating to Cllr Carter's conduct.
"His resignation has since been received and accepted by the Leader of Breckland Council, William Nunn."
Mr Carter was first elected to the Saham Toney ward in 2011. His details have already been removed from the council website.