The 20-year-old attacker's historic strike at the Caledonian Stadium was cancelled out by Billy Mehmet before Garry Brady netted in the closing stages.
Republic of Ireland Under-21 internationalist Rooney drilled in his first strike for the Highlanders following his £50,000 summer move from English Premiership new-boys Stoke City in a three-year deal.
Rooney was one of four players aged 20 or younger picked by Caley Thistle manager Craig Brewster as he opted for youth ahead of experience.
Inverness captain Grant Munro, who has not played in the SPL since injuring his knee on the opening day, missed out to 19-year-old Jamie Duff at the heart of the home side's defence.
Former Inverness hit-man Craig Dargo was benched for the Buddies, with boss Gus MacPherson preferring Jim Hamilton to partner Mehmet up front.
Inverness started the game brightly with 20-year-old striker Garry Wood missing an early chance moments before Ian Black fired a 30-yard screamer inches over the crossbar.
St Mirren weathered the storm as both sides settled into a midfield battle where chances came at a premium.
Hamilton went close for the visitors while 20-year-old Iain Vigurs shot wide for Inverness.
The breakthrough came two minutes before the interval when right full-back Ross Tokely found Wood, who was scythed down by Franco Miranda. Rooney sent Mark Howard the wrong way from the spot.
Black had a rasping shot saved before the break and one minute into the second half Rooney crashed a 12-yard rocket off the underside of the crossbar after being found by Don Cowie.
On the counter-attack, Hamilton went close with a powerful header. Wood could have doubled Inverness' lead on 54 minutes, but his 20-yard angled blast was pushed wide by Howard.
Mehmet equalised just after the hour when he lifted the ball over an onrushing Michael Fraser, after latching onto a Howard long ball that was flicked on by Gary Mason.
Howard's feet stopped Inverness regaining the lead in the 67th minute when he toed away a low defected shot from Rooney.
St Mirren forced their way back into the game after MacPherson replaced Steven Robb with Stephen McGinn.
McGinn beat Tokely down the wing with ten minutes remaining and his cross was blasted in by Brady for the winner.