DUP MLA Jim Wells has said that former party leader, the late Ian Paisley, would be "aghast" at the decision to run an openly-gay candidate.
Mr Wells was speaking after the party announced that Alison Bennington would run for the DUP in the upcoming council elections.
Ms Bennington will run for a seat on Antrim and Newtownabbey Borough Council.
After the announcement Ms Bennington said that she "regard(s) my private and family life as a matter for myself in the same way as everyone else".
However Mr Wells, who had the DUP whip withdrawn after criticising the party leadership, said the decision had been met with significant shock and hurt by many members who feel betrayed by the party over the issue.
He said that there was discontent from the top of the DUP, including MPs and MLAs to local members.
Mr Wells described the decision as his lowest moment in a 44-year of membership of the party and said it went against the values of the DUP.
The DUP has historically been seen as hostile towards the LGBT community. In the late 1970's then leader Mr Paisley led a 'Save Ulster from Sodomy' campaign in an attempt to prevent the decriminalisation of homosexuality in Northern Ireland.
Mr Wells has attracted criticism for his comments in the past, most recently banning two DUP colleagues from his social media for voting in favour of LGBT issues.
The former Health Minister alleged that Ms Bennington had been selected to run by party officers over more qualified local candidates.
"Nobody in the party beyond headquarters staff were aware of this," the South Down MLA said.
"I have had calls from every corner of Northern Ireland and further afield, from Londonderry, Kilkeel, Ballymena, Tyrone, all absolutely shocked on so many levels."
"There was absolutely no consultation with anybody at any level. It came as a complete shock to all except the leadership."
Mr Wells said that the party's Executive, Wesminster group and Assembly group received no prior notice of the decision.
He said that running an openly gay candidate was a "watershed decision" by the DUP leadership.
"This is a decision that totally undermines the ethos, tradition and history of the party," Mr Wells said.
"The party has always had a very clear view on family and social matters. When the story came out it hit like a bolt of lightning and rocked the membership in many areas to the core.
"There may be an element within the party that feels that the LGBT vote is a vote that can be secured, the problem is that in securing that they may well have alienated the huge core vote of the DUP which is Christian people who adhere to basic principals of family and marriage."
The DUP veteran said that he did not believe LGBT voters would move from other parties to the DUP.
"I am very personally angry and hurt by this decision, I have been a party member since 1975 and if Dr Paisley was still alive he would be aghast at this decision," Mr Wells said.
"I don't see any benefit in alienating and poking the eye of our core support, particularly in rural areas."
Mr Wells said that he believed the move would "backfire on the party" and had already left voters feeling "confused and let down".
The former Health Minister rejected the suggestion that his view could be seen as homophobic.
"People throw around that phrase willy-nilly, you can disagree with someone's lifestyle and still be friendly with them. People throw that word around like confetti to try and besmirch those with genuine views," he said.
"I believe the party still has a strong support base among church going people who believe that scripturally same-sex relationships are not acceptable, particularly in terms of representing the party.
"People can vote for the DUP, we don't discriminate, that's not the issue, the issue is the party had principles on these issues, as we have on protecting the unborn child and euthanasia, we have these core values."
Mr Wells said that he believed the decision could have long-term repercussions for the party, with many long-term members "soul searching" in the aftermath of the decision.
"It is such a radical change and has sent shockwaves around the whole party. In Belfast there may not have been a huge reaction, but in rural areas people feel let down and this is a bridge too far," he said.
"People were hurt by Arlene Foster's decision to attend a GAA match on a Sunday, but some understood why that had to be done even though it was painful. This one has gone way beyond that. A red line has been crossed by the party."
After the decision to run Ms Bennington was announced a DUP spokesperson said that the party believed she was an "excellent candidate and will make an excellent representative for the people of Glengormley".
"The party selects candidates on the basis of merit and we believe in equality of opportunity," the spokesperson said.