Former Ayr man Tom Walsh came back to haunt his old side as Inverness claimed three points in the Highlands to maintain their perfect start in the cinch Championship.
The midfielder's second-half goal – which bounced in off his chest after United had failed to clear a cross – summed up a frustrating day for the Honest Men.
David Hopkin's pre-match plans had suffered huge disruption when a number of Covid cases ruled four players out of the trip north.
The left-hand side of United's line-up was wiped out with Paddy Reading and James Maxwell both missing, along with keeper Aidan McAdams and Nick McAllister.
That meant three changes from last week's Premier Sports Cup tie against Dundee United and the reshuffled Ayr were almost behind just two minutes in when Michael Gardyne found space 12 yards out before flashing a shot just wide.
However, United could have hit the front on the break when Tomi Adeloye did well to make space in the box – but instead of pulling the trigger he played in Joe Chalmers and the chance was lost.
Clearcut chances were few and far between in the first half but it was Inverness who had the better opportunities.
Walsh worked a clever corner short on the left and his eventual ball was met by Shane Sutherland who headed wide as they probed for the opener.
Walsh almost turned provider again in 37 minutes when his corner was flashed wide by the head of Rory Deas.
But Ayr were proving a menace on the counter and Jordan Houston's cross only needed the slightest of touches at the backpost from Mark McKenzie, but the striker couldn't connect.
And at the other end, Rory Macgregor worked Caley's best chance on the stroke of half time with good work down the left before teeing up Walsh whose shot was well blocked by Chalmers inside the box.
But Caley came out quickly from the traps after half time and got the pivotal goal in the 54th minute.
Manny Duku's pace down the left stretched the Ayr defence and when his cross came in, Sean McGinty's attempted clearance flew up on to the chest of Walsh and looped past the helpless Charlie Albinson.
Ayr should have levelled quickly after great play down the left saw Aaron Muirhead feed Chalmers and his shot across goal only needed a touch, but Mikey Hewitt was inches away from connecting and the chance was gone.
But that was as good as it got for Ayr and although they threw on Jonathan Afolabi and Daire O'Connor from the bench, they could not test Mark Ridgers in the Caley goal.
And the hosts could have doubled their lead when both Walsh and Deas went close as the clock wound down.
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