The stonework is the giveaway. The 1874 station building is grey limestone from nearby Scarlett Point — the same quarry that supplied the original Port Erin station — and the footprint is an enlarged version of the wooden buildings used elsewhere on the line at Santon, Ballasalla and Colby. By 1903 it had been extended again, with a station master's office, ladies' and general waiting rooms, and an outside canopy added in 1910 to shelter passengers. The 1956 loss of the veranda and the winter 1993–94 restoration reshaped the interior, but the limestone shell is the same one the railway opened with. A blue heritage plaque went up on the building in August 2024, on the line's 150th anniversary, unveiled by former Chief Minister Tony Brown in the presence of the Lieutenant Governor.

The line has had a complicated history of partial operation, and four times Castletown has been the end of it. In 1967, when the Marquis of Ailsa reopened the railway after its 1966 closure, gas-main works to the south meant the station served as terminus that first season. In 1975 it filled the same role again, as a cost-cutting experiment that did not work — the train, the locals pointed out, no longer reached the capital. Major track and drainage works between 2000 and 2002 forced another temporary terminus, and from 2020 the long disruption of the COVID-19 pandemic kept services curtailed and the station's ticket office open chiefly to top up Bus Vannin travel cards. The pattern of the line for the last decade has settled on Castletown as the regular passing place for all timetabled trains, every two hours in standard season, more often when the calendar fills up.

The station has had its share of unlikely visitors. On 2 August 1972 a special train left Castletown with Queen Elizabeth II, the Duke of Edinburgh, Princess Anne, Prince Andrew and Prince Edward, and Lord Mountbatten in Royal Saloon F.36 (now preserved at the Port Erin railway museum), hauled by No.13 Kissack. Only the Queen Mother had been on a Manx train before. Seventeen years later the BBC dressed the station, in winter, with artificial snow and Russian luggage for a 1989 adaptation of Oswald Wynd's novel The Ginger Tree; locomotive No.11 Maitland was repainted matte black for the shoot. In 2000 the live-action Thomas and the Magic Railroad used the station as Shining Time Station, with the limestone clad in wooden boards and a brown-and-cream colour scheme, and Alec Baldwin and Peter Fonda working the platform. Five Children and It came in 2005, with Sir Norman Wisdom in the cast and a temporary canopy reinstated for the duration. Michael Portillo turned up in 2021 for Great Coastal Railway Journeys.

What keeps a small railway station looking like a railway station, rather than a tired shelter on a working line, is volunteer work. The Friends Of... group, formed in early 2009 by local residents and the resident station master, reinstated the waiting-room coal fire, put up a flagpole, repainted the benches, hung enamel signage, and won the commercial category of Castletown in Bloom in 2012. Their most ambitious project, an attempt to recreate the station's vanished advertisement hoarding on the up platform, ran from a 2016 planning permission through pandemic-era delays to a 2 August 2024 completion — a plaque unveiling on the 150th anniversary date itself, with sponsorship from Bushy's Brewery and funding from Culture Vannin. The hoarding now stands on the platform in approximately half its original length, with mooted plans to double it. In summer the platforms carry flower baskets and milk churns, a nod to the days when the station's cattle dock handled livestock right up to the final year of the full network in 1965.