Nearest rivals Swindon Town appeared poised to take top spot as they crossed to a 3-0 win at 10-man Notts Couny - Andy Williams netting a first-half brace before Liam Noble elbowed Nathan Thompson to see red and Massimo Luongo sealed the points.
But centre-back Ayling finished clinically from Luke Freeman's corner to keep City a point clear of Swindon at the summit and leave Crawley a place and two points above the drop zone.
There were bragging rights attached to the biggest win of the day as Gary Johnson masterminded a 4-0 win for Yeovil Town at Oldham Athletic, who are managed by his son Lee.
Stephen Arthurworrey opened the scoring after his header came back of the post and strikes from Simon Gillett and Sam Hoskins ensured Yeovil were 3-0 up after 40 minutes.
Kieffer Moore completed the rout from outside the box in the dying minutes as Yeovil closed the gap on Crawley and Oldham missed out on the chance to move into the play-off places.
Rochdale are sixth having been on the right side of a similarly comprehensive 4-1 scoreline at Colchester United.
Keith Hill's team are level on points with Oldham, Notts County and Peterborough United - the latter winning 2-1 at Leyton Orient to ruin Fabio Liverani's first game in the Brisbane Road hot seat.
The spoils were shared as fourth hosted third, with Preston North End defender Scott Wiseman volleying a 68th-minute equaliser at Deepdale after winger Carl Baker put MK Dons ahead.
It was the same scoreline at the Highbury Stadium as Fleetwood Town and fifth-placed Sheffield United both made it four games without a win.
Scunthorpe United are two points above the relegation zone after a 2-1 win over basement boys Crewe, a third win in four matches for Mark Robins' men, and Luke Norris scored both goals as Gillingham won at Doncaster Rovers by the same margin to remain level with United and a point behind their weekend opponents.
Bradford City and Coventry City were respective 1-0 and 2-0 winners at Chesterfield and Port Vale, while Jordan Cook notched a brace as Walsall saw off Barnsley 3-1.
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