The station, which is managed by ScotRail, is on the Ayrshire Coast Line, 41+1⁄2 miles (66.8 km) south-west of Glasgow Central.

[4] The glazed canopy that covers a small section of all four platforms and the waiting area was originally much larger than its current size.

In December 2006, the station received automatic ticket barriers as part of ScotRail's revenue protection policy.

[8] Its poor condition had necessitated an exclusion zone that covered a portion of the station platforms and tracks.

[9] On 25 September 2023, a severe blaze ripped through the building, destroying the roof and causing extensive damage to the interior.

The fire resulted in severe rail disruptions throughout the Ayrshire region, with stations inactive as far north as Irvine and as far south as Girvan.

[10] Ayr used to have an Intercity twice-daily London Euston service (one daytime and one sleeping car train) which ran to/from Stranraer via Barassie to the Glasgow South Western Line, which ceased in the early 1990s.

The Ayr to Glasgow service is one of the busiest on the rail network in Scotland and can suffer from serious overcrowding at peak times.

There are also less frequent services (operated by Class 156 DMUs) from Ayr to Girvan (roughly every two hours), Stranraer (six per day) and Kilmarnock (two-hourly).

There are also less frequent services (operated by Class 156 DMUs) from Ayr to Girvan (roughly every hour), Stranraer (six per day) and Kilmarnock (two-hourly).

[14] Stena Line passengers travelling on through "Rail & Sail" tickets to Belfast are provided with a free coach service direct from Ayr station to Cairnryan.