Leaf domatia, specialized chambers in the vein axils on the underside of leaves of many plant species, have remained an enigma for over a century. In this study we show a strong association between foliar domatia and mites in 37 plant species in Australasia. Overall, mites accounted for 91% of the arthropods observed in domatia. Across all species, a median of 51% of domatia were occupied and 71% of leaves showed mite evidence in domatia. The level of mite association did not depend on domatia type (pit, pouch, pocket, or tuft) or provenance (Papua New Guinea, Queensland, Victoria, or New Zealand). Mite association with domatia commonly varied between plant species, between individuals within species, and between shoots within individuals. The leaf developmental stage probably explains much of the variation in association for many of these species. The presence of a variety of life history stages of mites within domatia indicates that these structures act as shelters for development and reproduction. Furthermore, in 12 of 13 plant species examined, domatia concentrate mites in particular locations on the leaf. Mite taxa that we classify as largely predaceous (e.g. phytoseiids, stigmaeids and tydeids) or fungivorous (e.g. acarids and oribatids) were most common in domatia and dominated the association in 21 of 24 plant species in which the relative abundance of herbivorous, fungivorous and predaceous groups was quantified. We evaluate hypotheses that explain the role of leaf domatia, including non-functional hypotheses (e.g. architectural constraints), physiological function (e.g. gas exchange and water uptake), bacterial symbiosis and antagonistic and mutualistic associations with mites. Our quantitative results confirm anecdotal accounts of mite association with leaf domatia and are most consistent with Lundstroem's century-old hypothesis of plant-mite mutualism in which leaf domatia billet predaceous and fungivorous mites that prey on plant enemies. Leaf domatia are widespread among woody angiosperms and abundant in many temperate and tropical regions of Australasia. Mites, an ancient group of arthropods whose diversity and abundance parallels that of insects, are likely to be important selective agents on terrestrial plants. Our results (1) indicate that mite-domatia association represents a relationship of comparable scope to plant-ant associations mediated by specialized plant structures such as extrafloral nectaries, food bodies and specialized domatia; (2) suggest that sociality is not a necessary prerequisite for widespread and diverse mutualisms between arthropods and plants; and, (3) extend the diversity of organisms that produce specialized mite ‘houses’ from lizards, and wasps and bees to woody angiosperms.