The station was opened on 20 May 1875, as part of the Auckland and Mercer Railway on 20 May 1875, built by Brogden & Co,[4] when it was extended from Penrose.

[10] WAB Class locomotives were introduced to suburban services in 1922,[11] but the coaching stock appears from photos to have been unchanged in 1966.

[28] With increasing suburban traffic, work started in 1938 on a new ticket office,[29] carpark,[30] bridge and platform.

[33] Duplication of the tracks between Papatoetoe and Papakura started in 1929 as an employment relief scheme[34] and was completed on 29 March 1931.

[6] On 3 November 1986 Papakura closed to goods traffic, but re-opened temporarily in 1987 to take glass for recycling.

It had a bowstring footbridge connecting the platforms, which dated from at least the 1930s, constructed of old railway iron and sleepers.

This stopped in December 2014 when all Eastern Line trains began terminating at Manukau after the introduction of new timetables.

The heritage footbridge was demolished and scrapped, despite some local opposition,[35] and replaced with a concrete bridge with two passenger lifts.

Platforms were lengthened to enable six-car trains, because of anticipated growth in passenger numbers.

The building was refurbished and restored, and contains the preserved signal panel on display, a ticket office, public toilets and space for a coffee kiosk.

Since 3 February 2025, the basic weekday off-peak timetable is:[42] Papakura is served by bus routes 33, 365, 372, 373, 376, 377 and 378.