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Abstract The microbiome has been hypothesized as a driving force of phenotypic variation in host organisms that is capable of extending metabolic processes, altering development and in some cases, conferring novel functions that are critical for survival. Only a few studies have directly shown a causal role for the environmental microbiome in altering host phenotypic features. To assess the extent to which environmental microbes induce variation in host life‐history traits and behaviour, we inoculated axenicDrosophila melanogasterwith microbes isolated from drosophilid populations collected from two different field sites and generated two populations with distinct bacterial and fungal profiles. We show that microbes isolated from environmental sites with modest abiotic differences induce large variation in host reproduction, fatty acid levels, stress tolerance and sleep behaviour. Importantly, clearing microbes from each experimental population removed the phenotypic differences. The results support the causal role of environmental microbes as drivers of host phenotypic plasticity and potentially, rapid adaptation and evolution.