With five minutes of normal time remaining, the home side were trailing to Christian Eriksen's heavily deflected strike until Mauro Icardi and Matias Vecino netted in quick succession to turn the Group B encounter on its head.
Spurs were perhaps fortunate to see Eriksen's opener loop over Samir Handanovic off Miranda, but Mauricio Pochettino's side looked in little danger of relinquishing their lead heading into the final stages.
Inter were inspired by Icardi's moment of magic, however, the captain thundering a first-time volley into the bottom-left corner from 20 yards before Vecino nodded in Stefan de Vrij's header from a corner in the second minute of stoppage time.
INTER 2-1 TOTTENHAM— Inter (@Inter_en) September 18, 2018
THIS IS WHAT IT'S ALL ABOUT!!! #INTERISHERE
Late goals from @MauroIcardi and @vecino ensure a magical comeback win on the Nerazzurri's return to the #UCL. GET IN!!!! #FORZAINTER pic.twitter.com/MS1y2hDXix
It was a dramatic denouement to a largely scrappy affair, which had taken 37 minutes for either team to carve out a chance of any note - Harry Kane rounding Handanovic but then losing control after being picked out by Eriksen's majestic chipped pass.
That disappointment was swiftly overcome after the resumption, though, as a flat-footed Handanovic clawed unsuccessfully at Eriksen's effort, having got down smartly to keep out the initial shot.
And there was little sign of the late drama to come as Icardi thumped in Kwadwo Asamoah's cross from the left before Vecino was in the right place to secure Inter's celebratory return to European football's top table for the first time since 2011-12.
What it means: Pochettino's unwanted hat-trick
Pat on the back: Icardi proves Inter's inspiration
The Argentine was anonymous in the first half - his six touches were fewer than any other player - but his sensational volley galvanised both his team-mates and the stadium.
Boot up the backside: Spurs let it slip
With 84 minutes gone Spurs looked in no trouble. Although one can hardly legislate for Icardi's moment of brilliance, there was no man in a white shirt remotely near him. From that point on the momentum was with Inter.
Key Opta facts
- The last time Inter won their first Champions League group stage game was back in 2008-09.
- Eriksen has scored three goals in his last five Champions League appearances, one more than he netted in his previous 24 in the competition.
- Icardi has scored 108 goals for Inter in all competitions - only five of them have come from outside the box.
- Samir Handanovic played tonight his 250th match for Inter in all competitions.
Spurs will be desperate to avoid a fourth successive loss at Brighton and Hove Albion on Saturday. Inter, with only one win from four Serie A games this season, will head to Sampdoria with a spring in their step.