Commissioner Michael Murphy has conceded the force made mistakes and acknowledged a history of injustices against Indigenous Australians involving NT police.
"I am deeply sorry," he told Australia's largest Indigenous gathering at the Garma Festival at Gulkula, in northeast Arnhem Land, on Saturday.
Although the senior officer accepted he could not change or undo the past, he vowed to hold NT police accountable for harm inflicted in the past 150 years.
Mr Murphy said he would work to transform relations between police and Indigenous Australians and use his position to "make every effort to eliminate racism in the Northern Territory Police".
"I acknowledge this challenge will be hard … but the alternative is unacceptable," he said.
The Northern Australian Aboriginal Justice Agency welcomed Mr Murphy's apology as an important step towards the healing that needed to take place in the Territory.
"We are hopeful that these positive words are a catalyst for positive action to improve justice outcomes in the NT," an agency spokesperson said.
Aboriginal people were over-represented in the criminal justice system and Closing the Gap targets were not on track to be met, they said.
Mr Murphy also addressed the "profound and ongoing intergenerational impact" of colonisation and the "cruel and inhumane" decades-long practice of removing children during his address.
"Those impacts play a critical role in what causes disengagement, anti-social behaviour, offending and violence today," he said.
Mr Murphy, who took part in a Yolngu ceremony at the bunggul grounds following his speech, acknowledged the way forward could only be in partnership with Aboriginal Territorians and community-led organisations.
"I intend to develop a new relationship built on mutual respect, trust and human rights," he said.
A separate apology will be delivered to the remote community of Yuendumu, where Warlpiri man Kumunjayi Walker was shot dead by then-constable Zachary Rolfe in November 2019 during an attempted arrest.
The death sparked a murder inquiry and put the NT Police Force under scrutiny when evidence of racism was uncovered at a coronial inquest.
