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Cross-kingdom small RNA trafficking between hosts and microbes modulates gene expression in the interacting partners during infection. However, whether other RNAs are also transferred is unclear. Here, we discover that host plant Arabidopsis thaliana delivers mRNAs via extracellular vesicles (EVs) into the fungal pathogen Botrytis cinerea. A fluorescent RNA aptamer reporter Broccoli system reveals host mRNAs in EVs and recipient fungal cells. Using translating ribosome affinity purification profiling and polysome analysis, we observe that delivered host mRNAs are translated in fungal cells. Ectopic expression of two transferred host mRNAs in B. cinerea shows that their proteins are detrimental to infection. Arabidopsis knockout mutants of the genes corresponding to these transferred mRNAs are more susceptible. Thus, plants have a strategy to reduce infection by transporting mRNAs into fungal cells. mRNAs transferred from plants to pathogenic fungi are translated to compromise infection, providing knowledge that helps combat crop diseases. [Display omitted] • Arabidopsis delivers mRNAs via extracellular vesicles into fungal pathogen cells • Delivered host mRNAs are translated within fungal cells • Proteins translated from delivered host mRNAs reduce fungal infection • Knockouts in host genes corresponding to delivered mRNAs are more susceptible Exchange of small RNAs between host plants and their pathogens modulates gene expression in the interacting partners during host-pathogen interactions. Wang et al. show that the model plant Arabidopsis also delivers mRNAs within extracellular vesicles into fungal pathogen cells where they are translated and function to reduce infection. [ABSTRACT FROM AUTHOR]