In the past, when scientists encountered and studied ‘new’ environmental phenomena, they rarely considered the existing knowledge of First Peoples (also known as Indigenous or Aboriginal people). The scientific debate over the regularly spaced bare patches (so-called fairy circles) in arid grasslands of Australian deserts is a case in point. Previous researchers used remote sensing, numerical modelling, aerial images and field observations to propose that fairy circles arise from plant self-organization. Here we present Australian Aboriginal art and narratives, and soil excavation data, that suggest these regularly spaced, bare and hard circles in grasslands are pavement nests occupied by Drepanotermes harvester termites. These circles, called linyji (Manyjilyjarra language) or mingkirri (Warlpiri language), have been used by Aboriginal people in their food economies and for other domestic and sacred purposes across generations. Knowledge of the linyji has been encoded in demonstration and oral transmission, ritual art and ceremony and other media. While the exact origins of the bare circles are unclear, being buried in deep time and Jukurrpa, termites need to be incorporated as key players in a larger system of interactions between soil, water and grass. Ecologically transformative feedbacks across millennia of land use and manipulation by Aboriginal people must be accounted for. We argue that the co-production of knowledge can both improve the care and management of those systems and support intergenerational learning within and across diverse cultures.