Motherwell claimed their first win away from home in 2006 to re-ignite their push for the Bank of Scotland Premier League top six.
Richie Foran struck from the spot in the 51st minute after Ross Tokely had felled Alan McCormack inside the Caley area.
But the result moves the Fir Park club to within three points of the sixth-placed Highland club in the chase for the top half of the table.
But Caley had been the better team up until the penalty, but were denied an opener by a fine save from Well goalkeeper Colin Meldrum, who parried Dennis Wyness' fierce 34th-minute shot.
Inverness had created the first opportunity of the game after only two minutes though when Craig Dargo's flighted cross was met by Ian Black at the back post.
And the midfielder's header across goal had to be hacked off the line by Motherwell defender Stephen Craigan.
The home side continued to press forward and, three minutes later, Meldrum was caught in possession on the right-hand side of his penalty area by the sprightly Dargo.
But, while the striker effectively had an open net to aim at, his shot from an acute angle curled harmlessly over the crossbar.
Motherwell eventually threatened in the eighth minute courtesy of a Steven Hammell free-kick from 20 yards, but the left-back clipped his effort just wide as the game turned into a physical battle.
In the 22nd minute, Brian McLean's strong challenge on David Proctor resulted in the midfielder being carried off on a stretcher with a shoulder injury with his place taken by Alan Morgan.
But Caley continued to hold the impetus and Wyness made his presence felt for the first time four minutes later with a fine strike across goal from the edge of the area, which arrowed just wide of Meldrum's far post.
The home side definitely looked like the side most likely to break the deadlock and, 11 minutes before the interval, a fine run and cut-back from Hart allowed Wyness another effort on goal.
But, this time, his shot from 10 yards was brilliantly saved by Meldrum.
The second half started with Inverness claiming a penalty after substitute Morgan went down under a challenge from Martyn Corrigan.
But referee Steve Conroy waved play on and then cautioned the Inverness midfielder for unsporting behaviour.
However, Conroy then awarded a spot-kick to Motherwell after Tokely's foul on McCormack five minutes into the second half.
Foran took on the responsibility from 12 yards and comfortably beat Mark Brown with a low shot straight into the middle of the goal, while Tokely was booked for his misdemeanour.
Remarkably, Motherwell then had an appeal for a penalty dismissed when Scott McDonald went down under a challenge from Brown after Foran's deft lay-off.
The home side never recovered from the loss of the goal and, although they created late chances for substitute Graham Bayne and Wyness, the Steelmen resolutely held on to drag themselves back into contention for sixth place.
Teams:
Inverness CT Brown, Tokely, Dods, Munro, Hastings (Bayne 81),Hart, Black, Duncan (Keogh 70), Proctor (Morgan 24), Dargo,Wyness.
Subs Not Used: Fraser, Golabek, McCaffrey, Fox.
Booked: Morgan, Tokely, Black.
Motherwell Meldrum, Corrigan, Craigan, McLean, Hammell,McBride (O'Donnell 80), Kerr, McCormack, Foran (Paterson 87),Scott McDonald (McGarry 84), Clarkson.
Subs Not Used: Alexiou, Hamilton, Fagan, Kinniburgh.
Goals: Foran 51 pen.
Att: 3,183
Ref: S Conroy (Scotland).