Caley Thistle’s 2-1 defeat against rivals Ayr United means the Honest Men rather than the Highlanders will contest the play-off finals next week.
Inverness, who had six wins and a draw from their last seven Championship fixtures, needed a victory in this final night of regular league action.
However, the result means Ayr take second position, Queen’s Park third, with Partick Thistle fourth.
Dundee were crowned champions thanks to their thrilling 5-3 win against Queen’s Park in the winner-takes-all title showdown.
Former Ross County ace Josh Mullin’s first half strike deservedly had Ayr in front at half-time, but Nathan Shaw struck late on to set-up a grandstand finish.
However, there was still time for substitute Mark McKenzie to deliver the killer blow to take Ayr into the play-offs.
Inverness, who reached the Scottish Cup final against Celtic last week after beating Falkirk 3-0, stuck with the same starters.
Ayr arrived in the north on the back of a 1-0 win against Raith Rovers and their manager Lee Bullen made just one change, with on-loan Tranmere midfielder Reece McAlear, who was on loan at ICT last term, dropped to the bench as Ben Dempsey took his place.
Ayr were the first to try their luck as former Aberdeen midfielder Chris Maguire flashed a shot around the right post after some hesitation at the back.
There were many slack passes in the early stages and Maguire’s close-range effort was blocked by Wallace Duffy. Appeals for a handball were waved away by referee Don Robertson.
Home goalkeeper Mark Ridgers had to be alert as he tipped over a Mullin free-kick after Jay Henderson conceded a foul on Paddy Reading.
Inverness responded when Dan MacKay burst down the left and his cross was headed over the top by Billy McKay, who had to adjust his stance in order to find his range.
Maguire remained lively as he steered another low drive beyond the right post, with Ridgers diving to cover.
The nerves were evident and Caley Thistle were not quite as clinical as their opponents.
Ten minutes before the interval, Maguire released Mullin, who timed his run to perfection, raced through on goal and slid a shot past Ridgers.
There was an interval shake-up for the hosts as David Carson replaced Duffy at right-back and Dan MacKay made was for Austin Samuels. They switched from 4-4-1-1- to 4-4-2.
The fans needed to be patient as this was as tough a challenge as their team had faced all season.
Caley Thistle were almost back level on 53 minutes when Samuels swept play out to Billy McKay, who sent a cross back in for the striker, but he clipped his effort wide.
Samuels went even closer a minute later when his hooked shot looked net-bound until Frankie Musonda did enough to boot it off the goal-line. The mood was changing in their favour.
They kept pressing for an opening, but Ayr were well-drilled and limiting their options as the clock ticked down on their chances of turning it around as they so often do.
With 15 minutes to go, Sean Welsh fed the play out to St Mirren loan star Henderson and his cross was met by Carson, who crashed a drive just off target.
The game was on a knife-edge because another Ayr goal would have completely dashed their faint hopes.
However, ICT were level with eight minutes left when sub Lewis Hyde linked with Billy Mckay, who in turn played in Shaw for a close-range finish.
Both teams at this point knew they needed a winner and McKenzie was on hand to tap in from a pass from fellow sub Daire O’Connor.
Samuels stabbed the ball home late on, but the offside flag denied them one final flurry.
It was a cruel ending to what has been a terrific effort all round from ICT, but now they have the long wait for the season to end against Celtic in next month’s Scottish Cup final.
Caley Thistle (4-4-1-1) – Ridgers 6, Duffy 5 (Carson 46), Harper 6, Welsh 6 (Woods 79), Deas 6, Devine 6 (Delaney 73), Billy Mckay 6, Dan MacKay 5 (Samuels 46), Allardice 6 (Hyde 73), Henderson 6, Shaw 6.
Subs not used: Cammy MacKay (GK), Doran, MacGregor, Boyd.
Ayr United (4-4-2) – Albinson 6, Reading 6 (O’Connor 87), Musonda 6, McGinty 6, Murdoch 6 (Bryden 87), Dempsey, Akinyemi 6, Mullin 7 (McKenzie 76), Hewitt 6, Ashford 6 (McAlear 64), Maguire 7 (Mitchell-Lawson 76).
Subs not used: McAdams (GK), McAllister, Smith, Jenkins.
Referee – Don Robertson.
Attendance – 3,435.
Man of the match – Chris Maguire.
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