The first wave of resignations has seen six congregations quit, with half of the parishes in the Kirk's financial heartland. The controversy could have a bigger impact on Kirk coffers as more are expected to follow over the next two years.
In Edinburgh, Holyrood Abbey Church worshippers give £215,000 a year, New Restalrig gives £114,000 and St Catherine's Argyle collects £196,000, while Gilcomston South in Aberdeen, brings in £300,000 a year and on Lewis the Kinloch and Stornoway churches bring in £210,000 between them. In total, the Kirk brought in £60.5m in givings in 2011.
It is understood that wealthier traditionalist congregations who depart may offer less well-off parishes help if they wish to leave.
The developments came as father and son ministers said they would leave the Church over the move to allow congregations to ordain gay ministers made at its May General Assembly, despite the decision still having to be ratified. Rev David Randall of Ayrshire has followed his father Rev David Randall Snr of Logie St John's in Dundee in becoming the latest to say publicly that he will leave.
"I have always just felt it seems they are willing to pursue this liberalising pro-gay agenda regardless of the cost and it is emerging the cost is going to be very high. That is inevitable. There have been warning voices over the last three or four years that have just been ignored. It's very sad.
"It's interesting that the church is making statements about not being in crisis ... the fact they make those statements is quite revealing."
About 10 congregations are understood to be in negotiations with the Kirk to leave over gay ordination.
A Church of Scotland spokeswoman said: "The loss of any minister or member would be very disappointing given it is so early in the process of decision making on this matter, with a final decision not due until 2014 at the earliest.
"The Church of Scotland has an annual budget of around £120m. It is far too early to predict the precise effect of a drop in givings from the very small number of ministers and members who have given early indications of a wish to depart. We do not anticipate a serious effect on the budget and our overall finances."
Rebel Church of Scotland congregations are being wooed by the Free Church after they announced plans to quit the Kirk. The Free Church, which takes a strong traditionalist stance, is understood to have set up a working group to hold talks with congregations who are unhappy with the decision to allow gay ordination.
Logie and St John's Cross Church in Dundee has become the fifth to confirm its intention to leave the Kirk over the ordination of gay ministers.
In a statement it said: "Following the decision of the General Assembly on May 20 (to allow the ordination of openly gay ministers in civil partnerships), we have decided with deep regret that it is no longer possible for our congregation to remain within the Church of Scotland. The issue which we cannot accept is the Church's departure from its Scriptural foundation."
The Holyrood Abbey Church in Edinburgh, also announced its intention to leave last week.
Gilcomston South Church, Aberdeen, and St George's Tron Church, Glasgow, have already left the Kirk for similar reasons.