Maenofferen was first worked for slate by men from the nearby Diphwys quarry shortly after 1800. By 1848 slate was being shipped via the Ffestiniog Railway, but traffic on the railway ceased in 1850. In 1857 traffic resumed briefly and apart from a gap in 1865, a steady flow of slate was dispatched via the railway. The initial quarry on the site was known as the David Jones quarry which was the highest and most easterly of what became the extensive Maenofferen complex.

In 1861 the Maenofferen Slate Quarry Co. Ltd. was incorporated, producing around 400 tons of slate that year. The company leased a wharf at Porthmadog in 1862 and shipped 181 tons of finished slate over the Ffestiniog Railway the following year.

When the Ffestiniog Railway ceased operation in 1946, Maeofferen leased a short length of the railway's tracks between Duffws station and the interchange with the LMS railway, west of Blaenau Ffestiniog. Slate trains continued to run over this section until 1962, Maenofferen then becoming the last slate quarry to use any part of the Ffestiniog Railway's route. From 1962 slate was shipped from the quarry by road, although the internal quarry tramways including stretches of the Rhiwbach tramway continued in use until at least the 1980s.

The quarry was purchased by the nearby Llechwedd quarry in 1975 together with Bowydd, which also incorporated the old Votty workings: these are owned by the Maenofferen Company. Underground production at Maenofferen ceased during November 1999 and with it the end of large-scale underground working for slate in north Wales.