The Foxdale Railway was never a passenger venture dressed up. It existed to move lead. The line ran from an end-on junction with the Manx Northern Railway just west of St John's, looped north of the Isle of Man Railway station, then curved south to cross the IMR's Douglas line on an overbridge. This was the only place on the entire island where railway crossed railway above ground, a small distinction the line's enthusiasts have always loved. From there the track climbed at a steady gradient through Waterfalls Halt, the only intermediate stop, to a terminus at Upper Foxdale. Beyond the passenger platform the tracks pushed on into the mine workings themselves, where ore wagons could be loaded directly from the pit heads.

The Manx Northern Railway needed something stronger than its other locomotives to pull loaded ore wagons up the Foxdale gradients. The MNR bought one engine for the job. It was named Caledonia, after the company chairman's Scottish ancestry, and remains the only locomotive ever purchased for the branch. A second engine to the same design was proposed, to be named Atlas in connection with a never-built southern extension, but the line's finances never allowed it. One coach was also purpose-built for the branch and is now known simply as the Foxdale Coach. Both Caledonia and the coach survived the line. Both are still operational. Each summer the railway's annual events pair them again to recreate a Foxdale Line train, the original locomotive and original carriage rolling together as they did in the 1890s.

The line opened in 1886, almost exactly when the global lead market started to falter. The Foxdale Railway Company quickly went into liquidation. The Manx Northern Railway, which had leased the line from the start, was tied to its fortunes by lease terms that favoured the smaller company, so the larger railway found itself operating a money-losing branch on behalf of liquidators. Most of the MNR's freight revenue came from Foxdale, with wagons of lead heading to the harbour at Ramsey and coal and supplies returning. A Tynwald committee investigated the tangle. In the end, the Isle of Man Railway took over all operations on the Manx Northern Railway and was authorised, a few months later, to purchase both the Manx Northern Railway and the Foxdale line outright. The last working lead mine closed in 1911. From then on the line carried mostly spoil trains and the occasional passenger.

By the 1920s the Foxdale Station building had been converted into a private dwelling. The last regular passenger train worked the branch in 1940. Buses took over the service. World War II gave the line a brief second life with troop specials and occasional passenger trains run during bus shortages. The most lucrative work of all came from below ground: spoil from the Laxey and Foxdale mining areas was loaded at Foxdale, hauled along the line, then transferred to the north line for onward delivery to RAF Andreas, where it was used to build the runway. After that, the line carried very little. The final train was an engineering working that lifted rails and materials for use elsewhere on the system.

By the mid-1970s the rails were gone. The viaduct beyond St John's was demolished in 1975, and a further bridge later, for road widening. Today most of the route is a public walkway. The terminus structures at both ends survive. The St John's station building became a private dwelling, occupied for years by the well-known station master George Crellin until his death in 1976. The Foxdale terminus has lived several lives since closure, including stints as a youth club, the headquarters of the Manx Flux Co., and finally the Foxdale Heritage Centre. The stanchions of the old viaduct still stand. Some rails remain visible in the road at the outer terminus. The famous scissors crossing behind the station is said to be in place still, buried under a bank of hardcore. For years after the trains stopped, the spoil-strewn surroundings earned the area a nickname locals still remember: the back of the moon.