The third and current station was opened on 20 July 1846 by the Glasgow, Paisley, Kilmarnock and Ayr Railway[2] – this was connected to Ardrossan via Irvine two years later and to Carlisle via Dumfries & Gretna Junction in 1850.

The Dalry line remained in use for freight and occasional long-distance passenger trains until 23 October 1973, when it was closed to all traffic and subsequently dismantled.

Platform 4 is accessed via a subway and stairs or lift, and afforded only a bus stop style shelter although it does have a departure board.

Opened on by British Rail on 12 April 1976, it is a plain brick building containing an NX (entrance-exit) panel on the upper storey.

Kilmarnock signal box was severely damaged in a suspected arson attack on 25 December 2006 but was repaired and returned to full operation within weeks.

New sidings were installed in 2009-2010 along a short section of the trackbed of the old route to Dalry to facilitate the increased coal train traffic.

[6] In April 2012, the bridge's safety was upgraded after a man was seriously injured after jumping 40 ft from the top of the railway viaduct.

In 2011, the clock received a grant from the Railway Heritage Trust to undergo a regeneration scheme that began in late 2011 and was completed in March 2012.

[8] Despite an expensive upgrade in 2008,[9] it was announced in December 2022 following a full cabinet meeting of East Ayrshire Council that the station clock at the Kilmarnock railway station was to be removed and landscaped "with immediate affect" due to continuous technical difficulties preventing the clock and its LED lighting from working properly.

[10] Mondays to Saturdays Northbound, there are 2 trains per hour to/from Glasgow for most of the day with journey times taking between 40 and 50 minutes depending the service taken.

Westbound, there are 6 trains per day to Girvan, 4 of which continue to Stranraer, (and all call at Ayr) running a to a 2 to 4 hourly frequency (with peak extras).