Housing Minister Harriet Shing apologised for the dispossession of land and ongoing disadvantage faced by Aboriginal communities.
"We created Aboriginal homelessness and then we turned away from it, and for too long, we refused to even acknowledge that its existence and impact was our doing," Ms Shing told the Yoorrook Justice Commission on Monday.
"For that, I am sorry."
Indigenous Australians make up about three per cent of the population but account for one in five people facing homelessness nationally, according to census data.
The inquiry has heard 17 per cent of Aboriginal Victorians are seeking homelessness support and the figure is growing by 10 per cent a year.
Pushed to explain what her government was doing to improve ongoing disadvantage, Ms Shing pointed to the Victorian Aboriginal Housing and Homelessness Forum and Aboriginal Housing Victoria and noted she continued to advocate for more funding from the federal government.
"I'm not giving any impression that the system is perfect, but there is a lot happening," she said.
Housing Minister Harriet Shing gave evidence to the Yoorrook Justice Commission. (James Ross/AAP PHOTOS)
Commissioner Maggie Walter said housing forums had been operating for 30-plus years without appreciable change.
"Being told that the forum is meeting does not give myself ... any comfort that that is actually leading to change," Professor Walter said.
"It just seems like more bureaucracy to give the illusion of concern."
State and national, legislative, strategic and policy settings had underpinned adverse housing outcomes for First Peoples, Ms Shing said.
In the private rental market, Aboriginal people faced barriers such as racism and statistically lower incomes.
Ms Shing said the Aboriginal private rental assistance program provided up to $7000 for about 1000 families, but commissioner Anthony North questioned the adequacy of the grant.
"(It's) really pitiful, isn't it?" he asked.
"By providing, if you like, inadequate income support, you're setting up a system to fail, aren't you?"
The minister denied any government intention in the program's perceived shortcomings.
"(But) I think it does fail," Ms Shing said.
The work to undo decades and generations of disadvantage was slow and difficult, she told the commission.
"First Peoples deserved so much better and so much more than the contempt shown by successive governments," Ms Shing said.
Associate Professor Michelle Evans from the University of Melbourne said full social mobility for Indigenous Australians could still take decades.
"It's only really been a mere two generations since the 1967 referendum, which has instigated this ripple effect of change," she said.
"Of repeals, of legislations, and that have had a distinct controlling mechanisms around our family's abilities to build livelihoods that are independently driven."
An OECD report in 2022 said it can take up to five generations for people from disadvantaged backgrounds to achieve the mean income of a given society, Prof Evans said.
Commissioner Sue-Anne Hunter thanked Ms Shing for her evidence but said change wasn't happening quickly enough.