Dunfermline were relegated to Division One after a late goalkeeping error from Dorus De Vries and a deflection ended their seven-year spell in the SPL.
An error by Dorus De Vries allowed Inverness into the game
Inverness goalkeeper Michael Fraser had already produced a fine save to deny Adam Hammill before Jim McIntyre volleyed home after 37 minutes.
But, with Dunfermline looking nervous, De Vries allowed a Richard Hastings free-kick to slip through his grasp.
And a Rory McAllister drive flew in off Phil McGuire for an 89th-minute winner.
McGuire had come back into the Dunfermline back-four in place of the suspended Scott Wilson as they sought their fifth straight victory.
Ross Tokely made his 400th appearance for Inverness, replacing Stuart McCaffrey in defence, while Russell Duncan and Ian Rankin dropped out to make way for Markus Paatelainen and Ian Black.
Inverness held their own early on in a high-tempo game, but Dunfermline provided the first goal threat when a McIntyre effort from the corner of the penalty flashed just past the near post.
Craig Dargo had a chance at the other end, but De Vries made a comfortable stop from the snap shot.
Graham Bayne also fired wide for Caley Thistle when well placed.
But Inverness were being out-fought and out-thought and a 25-yard Hammill drive flew over the crossbar.
Michael Fraser was forced to tip another powerful Hammill shot over the crossbar following a surging run full of confidence.
Jim McIntyre (left) put Dunfermline ahead at Caledonian Stadium
And Dunfermline took the lead when Gary Mason's high ball was flicked into McIntyre's path by Tam McManus.
The former Dundee United player lashed a tremendous volley from 12 yards high into the Inverness net.
Sol Bamba came close to turning a cross from Hammill on target, only for Inverness to almost spring a surprise on the counter attack.
Richie Hart led the charge two minutes before the break. But, after exchanging passes with Dargo, the midfielder could only shoot straight at De Vries.
Hammill once again tested Fraser, this time with a swerving shot that produced a good catch from the Inverness goalkeeper.
A Bamba header flashed wide and Fraser did well to parry a McManus drive as Dunfermline remained on top after the break.
But Dunfermline conceded a free-kick as they looked to hold on to the lead with 13 minutes remaining.
And Hastings' free-kick was fired straight at De Vries only for the goalkeeper to allow the ball to slip through his grasp and into the goal.
With St Mirren having beaten Motherwell, Dunfermline could not afford to lose, but a cruel deflection sent them down.
Inverness CT: Fraser, Tokely, Dods, Munro (McAllister 76), Hastings, Hart, McBain (Sutherland 69), Black, Paatelainen (Wilson 61), Bayne, Dargo.
Subs Not Used: Ridgers, McCaffrey, Duncan, Rankin.
Goals: Hastings 77, McAllister 89.
Dunfermline: De Vries, Shields, Bamba, McGuire, Muirhead, O'Brien (Burchill 81), Mason, Glass (Owen Morrison 81), Hammill (McCunnie 66), McManus, McIntyre.
Subs Not Used: McKenzie, Young, Hamilton, Woods.
Goal: McIntyre 37.
Ref: M Ritchie