Labor has won the seats of Braitling and Katherine from former CLP chief minister Adam Giles and his former deputy, Willem Westra van Holthe.
Northern Territory Labor defeated the chief minister and his deputy but lost the seat it fought hardest for.
After the postal vote deadline on Friday, a final count revealed that Labor's Dale Wakefield had taken Braitling from former chief minister Adam Giles by 27 votes, the first time Labor has held the Alice Springs seat since the NT attained self-government in 1978.
In another first, Sandra Nelson seized Katherine for Labor from former deputy chief minister Willem Westra van Holthe by 28 votes.
But Deputy Labor leader Lynne Walker lost Nhulunbuy by seven votes to Yolngu independent Yingiya Mark Guyula.
That is a blow to the party, which was counting on her experience to help Chief Minister Michael Gunner lead an otherwise inexperienced government.
NT Labor President Syd Sterling said the party was considering a legal challenge.
"Our scrutineers are reporting more than enough inconsistencies and irregularities within the ballot process overall as to suggest you simply can't put your hand on the heart and say 'it is clear the will of the people has been expressed'," he said.
An emotional Ms Walker told Gove FM earlier this week that the result was "heartbreaking" but that "it's a very compelling thing for a Yolngu person to see one of their own family members running" on platforms of a treaty and a return to Yolngu law.
If this is the end of her political career, it is the loss of "a woman of great integrity, great strength, great compassion, and a terrific parliamentary performer whose skills and experience will be greatly missed," Mr Sterling said.
Mr Giles lsaid he expected the loss and wouldn't challenge the result.
He blamed his defeat on independents determined to see him go, electoral redistributions and the Don Dale youth justice abuse scandal.
"I was elected to fix the crime in Alice Springs, get the economy back up and running, fix tourism, and all those things have been done, so I'm quite satisfied I've been able to turn Alice Springs around," Mr Giles told AAP of his legacy.
"I think most certainly Alice Springs will go backwards."
CLP President Tory Mencshelyi has also resigned and said the thumping loss was disappointing, with only two members returned in a 25-seat Legislative Assembly, alongside five independents and 18 Labor.
She cited a lack of community consultation, political disunity, and countless scandals over the past four years as contributing factors.
But she wouldn't join former CLP leaders Shane Stone and Jodeen Carney, or former ministers Peter Chandler and Mr Westra van Holthe in demanding Mr Giles shoulder more of the blame.
"I think it was a shared responsibility," she said.
As the new Labor government looks to Sunday, when it will elect the rest of its cabinet, Ms Nelson said she didn't want a cabinet position and would turn one down if offered.