Both Arbroath and the Montrose branch had made successful £10,000 business support grant applications to Angus Council in July last year for help under the lifeline scheme.
However, they have now been told grants do not go to political parties and been ordered to refund the money.
It has now emerged that local branches may have been encouraged by a senior nationalist figure to play the system.
Social media posts from Dr Tim Rideout, part of the SNP’s policy development committee, appear to show members being encouraged to apply.
The convener of the Scottish Currency Group, Dr Tim appeared to write on Facebook: “I have made over £50k for the indy cause today”.
It is understood his posts did not relate to SNP activity and was not encouraged by the party.
Now the Scottish Conservative candidate for Angus South, Maurice Golden, has demanded answers.
He said: “This ruse has already resulted in the SNP paying back £20,000 for falsely claiming taxpayers’ money.
“Now that it has emerged that senior nationalists were actively encouraging local branches to play the system, it’s possible that other SNP outlets across the country will have benefited too.
“The SNP need to investigate how widespread this problem is and come clean about how much they claimed in total.
“If they won’t come clean, we may need a police investigation to examine if there has been an attempt at fraud here.
“This cash was designed to help honest businesses through a global pandemic which has cost thousands of lives in Scotland.
“Instead, the nationalists used it to line the pockets of their own selfish cause.”
A spokesman for the SNP in Angus said: "Arbroath branch has returned the funds in full.
“Montrose branch was advised last week that the payment was made in error and is in the process of contacting the council to do likewise."
An Angus Council spokesman said: “We do not comment on individual grant applications, but should we become aware of any issues we would seek to remedy the situation as appropriate.”