Fresh from a superb win against Premier League Hibernian, United fell to a first half opener from ex-Ayr man Andy Millen with a 24th minute strike which ultimately gave the Paisley Buddies victory.
The home crowd of 715 will take heart from an encouraging first half display by the Honest Men in which Saints keeper Craig Hinchcliffe pulled off a series of superb saves.
He denied John Maisano in the game's first real chance on 14 minutes when the Aussie played a neat one-two with Jerome Varielle before seeing his shot well held.
Saints replied with an opportunity for John Baird after he was sent through by the instrumental Millen but flicked his shot wide of the post.
Ayr were getting joy from the Maisano-Varielle partnership and the two combined once again on the edge of the box before Maisano saw his curling shot tipped wide at full stretch by Hinchcliffe.
The visitors struck their winner midway through the half when Millen drove home from the edge of the box after Baird and Stewart Kean saw efforts blocked by a desperate Ayr rearguard.
United's response was immediate with Andy Essler sweeping in a free kick which the dangerous Maisano headed towards goal but yet again he was denied by the in-form Hinchcliffe.
Maisano was at the centre of all Ayr moves and when he chested down Raymond Logan's 28th minute cross, Stuart Boyd lashed his shot straight at Hinchcliffe.
If the first half was flat, the second half was decidly low key with substitutions disrupting play and chances in short supply.
Saints came close with a Kirk Broadfoot free kick from 20 yards which curled just wide while Ayr's best effort came from the busy John Nolan who fired an effort wide from 25 yards.
Former home favourite Stewart Kean could have extended Saints' lead close to the end but he sent a header wide of the target from 10 yards.
Nolan looked the best of Ayr United’s newboys with Casey performing well when he came on late in the second half.
All in all his was still an encouraging performance by United
AYR: McGeown, McKinstry, Essler (Casey 72), McLaughlin, Campbell, Logan, Hyslop (Strain 62), Nolan (Reid 72), Varielle (Wardlaw 46), Maisano (Cashmore 46), Boyd (Robertson 46).
ST MIRREN: Hinchcliffe, Van Zanten, Broadfoot, Millen, Potter (McGowne 72), Maxwell, Murray (Reid 72), Reilly, Kean, Baird (McKenna 62), Corcoran (Lappin 64). Unused subs: Molloy, Smith.
Referee: John McKendrick. Crowd: 715