The governing Tories passed a law in 1977 making such trust funds illegal, but excluded their own party from the legislation in a grandfathering clause.
The Wildrose party called Wednesday on the Tories to shut down the fund and come clean.
"Every other political party in Alberta must reveal its assets. It's the law," Wildrose member Jeff Wilson said. "It's basic transparency. It's what Albertans expect and deserve."
The Progressive Conservatives created the fund in 1977 when Peter Lougheed was premier and the party controlled 69 seats in the 75-seat legislature.
It was first known as "P.C. Bill 24 Trust," but that name was changed in 1993 to "Tapcal Trust."
Drew Westwater, an Elections Alberta spokesman, said the trust fund is legal and the Tories have filed annual financial statements declaring how much money they have transferred from the fund to the party.
Disclosure documents filed with Elections Alberta suggest millions of dollars has been transferred over the years, including $513,713 in 1992 alone.
In some years, the amounts are listed as "Transfers from Trust." In others, they're simply called "Transfers."
There was also a period between 1994 and 2005 when the transfers were not included as separate line items in financial statements. The party then provided more detail for these years in 2006, at the request of the chief electoral officer.
In 2007, the party began filing separate letters that use the term "Tapcal Trust" when reporting the money transfers.
Westwater said under election financing law, the Tories do not have to disclose how much cash is in the trust.
"They are not required by law to tell us about the current status of the account. But if they transfer any funds to the party, they are required to provide that information to us, and they do that on an annual basis," he said.
Wildrose party officials first came across the term "Tapcal Trust" last year in Tory party financial statements filed for 2012, and asked Elections Alberta for more details.
New Democrat Rachel Notley said the existence of the trust raises questions about which corporations or individuals made donations to the fund and whether they were legal.
She said Albertans also need to know if the cabinet made decisions over the years that could have affected the wealth of the trust.
"The whole purpose of elections finance laws is to ensure that Albertans know who is funding political parties and to at least attempt to create a level playing field for the parties," she said.
"That the government would write laws that give them an unfair advantage over other political parties is perhaps even more offensive than the advantage itself."
Officials with the Progressive Conservative Party of Alberta did not respond to requests for comment.
However, party president Jim McCormick defended Tapcal Trust in an email to party members late Wednesday afternoon.
"There has been some recent confusion over our Tapcal Trust," he wrote.
"The Progressive Conservative Association of Alberta has stewarded monies raised prior to changes in political fundraising legislation so that the funds remain intact today in the form of a trust."
McCormick goes on to explain that any money drawn from the trust was done under the law and reported to Elections Alberta.
He also boasts that the party raised more than $4.4 million last year, and appeals for more donations to prepare for the 2016 election.
Westwater said chief electoral officers over the years have reviewed the trust fund.
"Up until now the CEOs have ruled that it is a valid trust account that was a legitimate account to transfer funds to the PC party," he said.
"We have a new chief electoral officer that has not reviewed it currently, but I'm sure that we will be looking at it again."
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