The former Labor leader and defence minister said that the displays in the museum section of the Memorial would be "revised" when the work of reconstructing the expanded institution is complete.

"We do have to have a proper recognition of the frontier conflict", he said.

"All the additions to the memorial which are huge will be completed by 2028, and that's when we'll see the revised display related to the Frontier Wars."

The policy on giving greater recognition to the resistance to colonisation emerged quietly in a press conference in October about other, unrelated matters.

The previous chairman of the War Memorial's governing council, the former Liberal defence minister Brendan Nelson, said then that there would be a "much broader, a much deeper depiction and presentation of the violence committed against Indigenous people, initially by British, then by pastoralists, then by police, and then by Aboriginal militia. We will have more to say about that in due course".

Previously, the line had been that the Frontier Wars were best depicted in other museums.

Mr Nelson's successor, Kim Beazley, underlined that change of policy on ABC radio this week. He said that this greater recognition of resistance to British colonisation should be reflected across the country.

"We have to have the Frontier Wars depicted in every museum - in all the state museums and in the Australian museum, and we have to be prepared, as we go through truth-telling processes, to consult with different Aboriginal nations as to how they want massacres reflected - commemorated."

On some credible estimates, at least 20,000 Indigenous Australians died in the conflicts with colonial soldiers, police and settlers' militias from 1788 to 1928.

The issue has become a political flashpoint since the Albanese government signalled last year it would expand the exhibition as part of a $500 million redevelopment, drawing criticism from conservative politicians.

The war memorial's freshly-appointed chair agreed on ABC radio that many Australians had been "taught a fiction".

While the curating committee for the expanded exhibit won't be finalised until next year, Mr Beazley said it would "acknowledge" massacres of Indigenous Australians alongside the battles and resistance between colonialists and First Nations people over the centuries.

"What I think we will do at the memorial is give the Aboriginal population the dignity of resistance," Mr Beazley told ABC on Monday.

"For years, we conned ourselves that there was no resistance - there was a hell of a resistance."

It's expected the full expanded collection will be completed by 2028, Mr Beazley said.

The memorial chair said extra funding would likely speed up the process but didn't believe the federal government was in a budgetary position to "pass money around".

READ MORE:

Veterans' Affairs Minister Matt Keogh announced in September last year cultural institutions had a responsibility to reflect on frontier conflicts.

"The recognition and reflection on frontier conflict is something that is a responsibility for all of our cultural institutions, not just here in Canberra, but across the country," he said.

"It's important that we do raise awareness for people across the country about the importance of frontier conflict and the impact that that had on our First Nations people and to properly reflect upon and understand our history."

Former war memorial chair Brendan Nelson said the memorial council had decided to grow the institution's displays on frontier conflicts.

It would show a "much deeper depiction and presentation of the violence committed against Aboriginal people, initially by British, then by pastoralists, then by police, and by Aboriginal militia", he said.