A gallery should display both sides of the conflict, including the resistance of First Nations "guerillas", new chairman Kim Beazley said.
The new leadership at the memorial has already said there should be recognition of the Frontier Wars, in which British colonial forces fought and killed Indigenous people.
But Kim Beazley has now spelled out to ACM, publisher of this newspaper, this depiction of the Frontier Wars should not be a passing reference but a substantial part of the revamped galleries. It should not just be from the invaders' perspective but also from that of what he termed "guerillas".
"My view is that we need to have a focus on Aboriginal guerilla campaigns," he said.
"This should be in a special section of the galleries in the museum section of the memorial.
"There was a substantial level of self-defence. There were terrible massacres and also more structured wars. There was very good Aboriginal leadership. Sometimes there were peace discussions.
"Aboriginal people need to be given the dignity of resistance, and not just assumed that they were the passive recipients of injustice."
But a former principal historian at the Australian War Memorial remained uneasy about the promises.
"The problem is that the memorial hasn't been consistent. It looks like the Australian wars could end up being just a showcase in a colonial gallery," said Peter Stanley, of the University of NSW in Canberra.
Between 20,000 and 80,000 mostly Indigenous people were killed in the wars between Indigenous people and the forces of the colonists, whether as soldiers, police or vigilantes.
In contrast, Australia sent soldiers to Sudan in 1885. Only nine of them died from disease, and not from battle, so to put a display on the Frontier Wars alongside one on Sudan would be far from proportionate, Prof Stanley believed.
He said there should be a truly substantial coverage at the memorial of the Australian wars.
"The memorial should stop ducking and weaving and obfuscating. They've come out with all sorts of bizarre calculations, and all of them are shonky," he said.
"The memorial has got to come clean on this. It's got to follow the facts of history and what the community expects.
He did, however, welcomes Mr Beazley's apparent enthusiasm for full coverage of the Frontier Wars, saying: "He wants to tell the truth about our history and I acknowledge and applaud that."
One of the Aboriginal advisers to the memorial also wants a fuller recognition of the frontier conflicts.
"It was a war," said Frank Lampard, who is on the AWM's Aboriginal and Torres Strait Islander Advisory Group.
"The truth is that there was so much violence. It did take place. It's a truth-telling story so it's got to be a part of the Australian story."
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