The Buddies' Lawrence Shankland missed a second-half penalty before Paul Cairney gave Ayr the lead.
But the Honest Men were reduced to 10 men with a red card for Jamie Adams.
And, within three minutes, St Mirren were level through a Sutton header and Ryan Hardie came close to a winner with a shot off the Ayr crossbar.
It was a game after which the home side will be disappointed not to have maintained their recent winning run.
With the visitors content to hit on the break, it was St Mirren who had the majority of the first-half chances, including a Gary MacKenzie header cleared off the line.
Despite the home dominance, Ayr were creating chances, but the big talking points came after the break.
St Mirren spurned the opportunity to go in front from the spot after 59 minutes when Jason Naismith was brought down and Shankland screwed the penalty low past the post.
The miss was compounded five minutes later when Ayr took the lead with a clinical finish from Cairney for his third goal of the season.
Adams received a straight red card from referee Greg Aitken after 77 minutes for a foul on Kyle McAllister and substitute Sutton soon contributed his eighth goal of the season from David Clarkson's cross.
Hardie smashed a 20-yard effort off the crossbar as the home side pressed for the win.
However, the Buddies had to make do with a second 1-1 league draw with Ayr this season, while the visitors drop to second bottom following Dumbarton's win over Falkirk.
St. Mirren manager Jack Ross: "We had a lot of opportunities to win the game, but if we can keep picking up seven points out of nine from each three-game segment over the next few weeks, we will certainly climb the table.
"Our reaction to going a goal down was good, but the players are frustrated not to continue the winning run."
Ayr United manager Ian McCall: "Under the new rules, the red card for Jamie Adams was probably correct - one of the few decision the officials got right.
"The decisions cost us two points and the players a win bonus."
Match ends, St. Mirren 1, Ayr United 1.
Second Half ends, St. Mirren 1, Ayr United 1.
Attempt saved. John Sutton (St. Mirren) header from the centre of the box is saved in the top centre of the goal.
Corner,  St. Mirren. Conceded by Ross Docherty.
Attempt missed. Stephen Mallan (St. Mirren) right footed shot from outside the box misses to the right.
Corner,  St. Mirren. Conceded by Ross Docherty.
Attempt missed. Stephen Mallan (St. Mirren) right footed shot from outside the box is too high.
Attempt missed. Kevin Nisbet (Ayr United) right footed shot from the right side of the box misses to the left.
Foul by David Clarkson (St. Mirren).
Ross Docherty (Ayr United) wins a free kick in the attacking half.
Corner,  St. Mirren. Conceded by Greg Fleming.
Attempt saved. Ryan Hardie (St. Mirren) right footed shot from outside the box is saved in the top centre of the goal.
Goal!  St. Mirren 1, Ayr United 1. John Sutton (St. Mirren) header from very close range to the centre of the goal. Assisted by David Clarkson.
Corner,  St. Mirren. Conceded by Robbie Crawford.
Corner,  St. Mirren. Conceded by Scott McKenna.
Substitution, St. Mirren. Ryan Hardie replaces Andy Webster.
Substitution, Ayr United. Michael Rose replaces Gary Harkins.
Attempt missed. Stephen Mallan (St. Mirren) right footed shot from outside the box is just a bit too high from a direct free kick.
Jamie Adams (Ayr United) is shown the red card.
Kyle McAllister (St. Mirren) wins a free kick in the attacking half.
Foul by Jamie Adams (Ayr United).
Attempt missed. David Clarkson (St. Mirren) header from the centre of the box is close, but misses to the left following a corner.
Corner,  St. Mirren. Conceded by Greg Fleming.
Attempt saved. Kyle McAllister (St. Mirren) left footed shot from outside the box is saved in the top left corner.
Substitution, Ayr United. Kevin Nisbet replaces Alan Forrest.
Substitution, Ayr United. Patrick Boyle replaces Daryll Meggatt because of an injury.
Attempt missed. Stephen Mallan (St. Mirren) right footed shot from outside the box is high and wide to the left.
Substitution, St. Mirren. David Clarkson replaces Lawrence Shankland.
Conrad Balatoni (Ayr United) is shown the yellow card for a bad foul.
Lawrence Shankland (St. Mirren) wins a free kick in the defensive half.
Foul by Conrad Balatoni (Ayr United).
Goal!  St. Mirren 0, Ayr United 1. Paul Cairney (Ayr United) right footed shot from the centre of the box to the bottom right corner. Assisted by Jamie Adams.
Delay in match Jason Naismith (St. Mirren) because of an injury.
Attempt blocked. Lewis Morgan (St. Mirren) right footed shot from the centre of the box is blocked.
Gary Mackenzie (St. Mirren) wins a free kick in the attacking half.
Foul by Gary Harkins (Ayr United).
Substitution, St. Mirren. John Sutton replaces Rocco Quinn.
Penalty missed! Bad penalty by Lawrence Shankland (St. Mirren) right footed shot is close, but misses to the left. Lawrence Shankland should be disappointed.
Ross Docherty (Ayr United) is shown the yellow card.
Paul Cairney (Ayr United) is shown the yellow card for a bad foul.
John Sutton's equaliser for St Mirren ensured that they and visitors Ayr United occupy the bottom two spots in the Scottish Championship.