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Abstract PremiseThe ability of plants to adapt or acclimate to climate change is inherently linked to their interactions with symbiotic microbes, notably fungi. However, it is unclear whether fungal symbionts from different climates have different impacts on the outcome of plant–fungal interactions, especially under environmental stress. MethodsWe tested three provenances of fungal inoculum (originating from dry, moderate or wet environments) with one host plant genotype exposed to three soil moisture regimes (low, moderate and high). Inoculated and uninoculated plants were grown in controlled conditions for 151 days, then shoot and root biomass were weighed and fungal diversity and community composition determined via amplicon sequencing. ResultsThe source of inoculum and water regime elicited significant changes in plant resource allocation to shoots versus roots, but only specific inocula affected total plant biomass. Shoot biomass increased in the high water treatment but was negatively impacted by all inoculum treatments relative to the controls. The opposite was true for roots, where the low water treatment led to greater proportional root biomass, and plants inoculated with wet site fungi allocated significantly more resources to root growth than dry‐ or moderate‐site inoculated plants and the controls. Fungal communities of shoots and roots partitioned by inoculum source, water treatment, and the interaction of the two. ConclusionsThe provenance of fungi can significantly affect total plant biomass and resource allocation above‐ and belowground, with fungi derived from more extreme environments eliciting the strongest plant responses.