A David Raven own goal and Niall McGinn’s close-range finish overturned Edward Ofere’s opener for the home side, as the 2-1 win guaranteed Aberdeen will finish no lower than second place in the Scottish Premiership.
Dundee United can halve the gap to Inverness in third to three points should they beat Celtic at Tannadice on Sunday.
The fixture marked a welcome return to league action for Inverness, whose cup success had been overshadowed by the handball controversy that engulfed Scottish football this week.
Inverness made one change from the side that beat Celtic in the Scottish Cup semi-final.
Ross Draper missed out through suspension and Nick Ross came in his place.
Aberdeen were without Barry Robson, who was banned by an SFA tribunal on Thursday. In Robson’s absence, Ryan Jack stepped into the centre of midfield.
Inverness continued with two up front, as they did for the semi-final victory, with Marley Watkins and Ofere deployed together.
It was Watkins who had the first chance of the game 13 minutes in as he latched on to Nick Ross’ through-ball. Aberdeen goalkeeper Scott Brown was out quickly, however, and charged down Watkins’ effort.
Neither team could get a grip on possession in the first half as much of it was spent trying to get the ball down. Inverness had plenty of the ball at the back but were struggling to get Ofere and Watkins in behind.
Aberdeen had one half chance through former Inverness striker Adam Rooney, who skewed wide under pressure from Josh Meekings, before McGinn drilled straight at Ryan Esson.
The hosts had a great chance through Ross, who shot straight at Brown when one-on-one after Christie played him in.
But the best opportunity came on the half-hour when Graeme Shinnie broke away on the left flank and squared for Watkins, who was unmarked on the six-yard line.
A solid connection and Inverness would have been one up, but the Welshman tamely sidefooted it and Brown sprawled across to make the save.
Watkins wasted another chance before the break, blazing over when Meekings – the man at the centre of the recent handball controversy – dropped a ball over the top of the Dons defence.
For all their chances wasted in the first half, Inverness finally made their momentum count when Ofere gave them the lead four minutes into the second period. Watkins crossed for the Nigerian striker, whose initial header was blocked by Brown but, while lying on the ground, Ofere managed to scoop the ball into the net.
The visitors hit back immediately and saw Jack draw a superb save from Esson, which preceded a goal-mouth scramble that Aberdeen believed warranted a penalty for handball.
Their equaliser came with just over 20 minutes to go as McGinn’s in-swinging free-kick glanced off the head of Raven and crept inside Esson’s far post.
Aberdeen were swiftly in front. Jonny Hayes’ corner found Rooney, whose effort was blocked on the line by Gary Warren but McGinn was on hand to turn in the rebound.
Despite late huffing and puffing, Inverness were unable to break down a stubborn Aberdeen rearguard again.