Indigenous Affairs Minister Nigel Scullion has questioned the organisation's relevance to Aboriginal people - while Congress says it's more relevant than ever.
It was established as a voice for First Australians - but now that voice could be silenced.
Indigenous Affairs Minister Nigel Scullion made it clear the government had abandoned support for the elected body.
He has told CAAMA radio the government won't provide anymore funds to the National Congress of Australia's First Peoples.
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"The deal was 30 million dollars and they would be self-funded after that, because they would be independent of govt. There's no point coming back after frankly years of inactivity saying well we've spent the 30 million - that was all a bit of a misunderstanding - can we have some more?"
Former Aboriginal and Torres Strait Islander Social Justice Commissioner Dr Tom Calma was instrumental in setting up Congress in 2010.
He says it had always strived to be self-sufficient but needed a decade of government funding during the establishment phase.
"Within 10 years we believed that we could be totally self-autonomous, we didn't need to get supported by govt and we'd have the funding base to be able to go forward, and I think that's still our aspiration, but unfortunately a change of govt, a change of position."
Around the world there are various models of indigenous representation.
In the United States, the National Congress of American Indians is financially independent while Canada's indigenous peoples are represented by the Assembly of First Nations - an independent body funded by government.
New Zealand has dedicated indigenous seats in parliament as well as a range of government bodies representing Maori interests.
Historically, Australia has struggled to establish a self-governing body for its First Nations people.
In 2004, the Howard government abolished the Aboriginal and Torres Strait Islander Commission - in favour of a government-appointed advisory body.
National Congress was supposed to be that body but now the Indigenous Affairs minister has cast doubt over whether it truly represents Aboriginal people.
"I talk to Aboriginal people right across this country, and all the time I spend my life with Aboriginal people - the vast majority of them say we just don't even hear from them, we don't know who congress is."
But what was the opinion on the streets of Redfern in Sydney's Aboriginal heartland?
"Have you heard of the National Congress of Australia's First Peoples?"
"Of course I have. I'm a part of it."
"You're a part of it?"
"Yeah."
"Have you ever heard of the National Congress of Australia's First Peoples?"
"Umm to be honest no."
"Do you think they're an important body?"
"I'm a member. Absolutely."
Congress has around 8,500 members and 180 member organisations.
It is only a small fraction of the indigenous population of half a million people.
But it has wide reach across the country.
Though it's still pushing to increase that membership, co-chair Rod Little is adamant that Congress is more relevant than ever - especially as debate continues around Constitutional Recognition.
Mr Little says the body is still determined to be self-funded in the future and adds the Congress of American Indians took 30 years to get established, and is now virtually independent and self-sufficient.
Mr Little believes the Congress needs a little more time and money to also become self-sufficient.
"The key thing that the PM said to us that he wanted to have a relationship, wanted to do things with first peoples, not to first peoples. And so we just want that to happen, we want to give that a chance, not cut us off at the knees."
