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The unprecedented price inflation of Black truffles, recently exceeding 5000 Euro kg(-1) (in Zurich), is a combined result of increasing global demands and decreasing Mediterranean harvests. Since the effects of long-term irrigation and climate variation on symbiotic fungus-host interaction and the development of belowground microbes are poorly understood, the establishment and maintenance of truffle plantations remains a risky venture. Using 49 years of continuous harvest and climate data from Spain, France and Italy, we demonstrate how truffle production rates, between November and March, significantly rely on previous June-August precipitation totals, whereas too much autumnal rainfall affects the subsequent winter harvest negatively. Despite a complex climate-host-fungus relationship, our findings show that southern European truffle yields can be predicted at highest probability (r = 0.78, t-stat = 5.645, prob = 0.000 01). Moreover, we demonstrate the reliability of national truffle inventories since 1970, and question the timing and dose of many of the currently operating irrigation systems. Finally, our results suggest that Black truffle mycorrhizal colonization of host fine roots, the sexualisation of mycelium, and the formation of peridium are strongly controlled by natural summer rainfall. Recognising the drought-vulnerability of southern Europe's rapidly growing truffle sector, we encourage a stronger liaison between farmers, politicians and scientists to maintain ecological and economic sustainability under predicted climate change in the Mediterranean basin.