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Summary Arbuscular mycorrhizal fungi (AMF) are critical to native plant community ecology and influence plant invasions. Research has focused on nutritional benefits of AMF, although evidence shows that they may also confer pathogen resistance. However, most such work has focused on agriculturally relevant plant species. Therefore, whether AMF confer pathogen resistance tonative(wild) plant species, and impact of novel plant–microbial relationships on this benefit, remains understudied.We conducted a series of experiments measuring mycorrhizal‐induced resistance (MIR) to pathogens in native prairie plant species. We tested for pathogenicity across 69 field‐isolated fungi and oomycetes across five plant species. We then conducted experiments assessing growth response to native and non‐native AMF and pathogens in three plant species from native populations and milkweed (Asclepias syriaca) from native and postagricultural populations.We found evidence of MIR in milkweed. Moreover, we identified differential effects of AMF depending on plant species, with milkweed from native populations showing benefits from AMF. Finally, growth response was mediated by local adaptation, with matching AMF–pathogen origin strengthening responses.This work illustrates the importance of locally sourced AMF and plants to native plant ecology and suggests that pathogen resistance may be an important dimension of AMF benefit.