The Thunder led at every change, and withstood Metro's late charge to record a memorable 15.10 (100) to 11.16 (82) victory.
The players were ecstatic after the game, singing the team song on the ground in front of their faithful fans.
For the Thunder, Anthony Tipungwuti and Damien Barry's run and carry was influential in setting the tempo for their side and Jake Neade was excellent in the clinches.
Ben Rioli and Willy Rioli, cousins of Hawthorn's Cyril, wreaked havoc all night and 2011 under-18 All Australian Jed Anderson was another major instigator in the win.
Urged on by their home crowd, the Thunder's relentless pressure was evident early in the game and it seemed to trouble the Metro team.
The Thunder tackled ferociously, setting a match-defining standard in the first half, and caused Vic Metro to cough up the ball at inopportune times.
Metro's Luke McDonald, son of North Melbourne's Donald, fought valiantly for his side, alongside Ben Lennon and Nick Vlastuin, despite the Thunder's strong intent.
The Thunder's tackling onslaught continued in the second half, as they forced the Metro players to earn every possession.
Ashlin Brown, though, was a constant threat up forward for Vic Metro with four goals and Lennon (two) was also amongst the best.
Metro clawed back to within a couple of goals in the final term, although the night belonged to the Thunder in what AFL talent manager Kevin Sheehan described as "one of the greatest wins in the team's history".
The Thunder will take a lot out of defeating the division-one powerhouse, despite Metro missing star players Joe Daniher (Essendon father-son in waiting), Liam McBean and Jonathan O'Rourke.
Territory coach Brendan Toy was delighted with the pressure his team applied and praised his players for their work rate.
Metro coach Rohan Welsh will look to address the disposal efficiency of his side and will demand quick improvement in the side's next match against South Australia on June 16.
The Thunder's next game is also against South Australia on June 10.
NORTHERN TERRITORY 3.3 7.5 11.8 15.10 (100)
VIC METRO 1.8 3.9 5.13 11.16 (82)
GOALS
Northern Territory: Autio 2, Ankers 2, W Rioli 2, McLean, Assan, Anderson, Barry, McEwin, Renehan, B. Rioli, Tipungwuti, Williams
Vic Metro: Brown 4, Billings 3, Lennon 2, Hrovat, Langdon
BEST
Northern Territory: Tipungwuti, B Rioli, W.Rioli, Anderson, Neade, Lawton, Barry
Vic Metro: Brown, Billings, Hrovat, McKenzie, Lennon, Jaksch
