Michael Murphy told attendees at the Garma Festival that the force had "made mistakes", apologising for the past harms and injustices to all Aboriginal Territorians.
He addressed the role police had played in enforcing the Howard government-led intervention, acknowledging many Aboriginal people had viewed the measures as "racist and reminiscent of the old Protection Era."
NT Police Commissioner Michael Murphy apologised to the Indigenous community at Garma. (Mick Tsikas/AAP PHOTOS)
But Mr Howard on Saturday defended the measures introduced during his administration.
"The intervention was totally justified because the NT government had failed in its responsibility to Indigenous children in the Territory, despite the findings of a report that that government had commissioned," he said in a statement.
"The Rudd government seriously weakened the intervention.
"That should not have happened and I stand by every element of my government's decision to intervene."
Enacted in 2007 across 77 Aboriginal communities, the intervention included restrictions on alcohol and pornography, the quarantining of welfare payments through the BasicsCard and the cancelling of a community employment program.
The Liberal government introduced legislation to enable the measures that suspended the application of the Racial Discrimination Act.
Mr Murphy said while some Aboriginal people had appreciated the police presence, the intervention had reduced customary laws and cultural practices.
He said police needed to be accountable for the past treatment of Indigenous people and pledged his force would work to prevent further harm.
"At times, police officers have abused their powers or fallen short in their duty of care towards Aboriginal offenders, witnesses and victims of crime," he said during his Garma address in northeast Arnhem Land.
"I intend to develop a new relationship built on mutual respect, trust and human rights."
The Racial Discrimination Act 1975 was suspended as part of the NT intervention measures. (Terry Trewin/AAP PHOTOS)
Mr Murphy's comments drew heavy criticism from the Northern Territory Police Association.
The union's acting president Lisa Bayliss said while it was important to "confront, acknowledge and learn from the past", it must not define the Territory's police force.
"It is also not the role of police to assess the success or otherwise of federal government-directed policies of Closing the Gap, the stolen generation and the intervention, as the commissioner has done," she said.
Mr Murphy subsequently resigned from the union, saying he was "incredibly disappointed by the statements" but was proud to serve as commissioner.
His apology was welcomed by Prime Minister Anthony Albanese and Indigenous groups including the Northern Australian Aboriginal Justice Agency.
The force's new direction will also involve the development of an "anti-racism strategy" led by Leanne Liddle, the most senior Indigenous employee at NT Police.
