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Abstract Previous studies showed that dipping rice roots in a formulation of Trichoderma asperellum at the transplanting stage or applying the strain as a foliar spray post transplanting led to a statistically significant reduction in rice blast (caused by Magnaporthe oryzae ) and increased grain yield in Tanzania. We investigated the effect of dipping at transplanting or post‐transplanting spray application on the root‐associated microbiome or leaf epiphytes via amplicon sequencing, and on plant responses via RNA‐seq. Both root dipping and foliar application with T. asperellum spore suspension only had a limited impact on the leaf epiphytes and root/rhizosphere microbiome after 1 and 4 weeks of treatment, respectively. However, both treatments led to notable and persistent changes in plant responses in leaves. Moreover, root dipping led to greater and more persistent changes in plant responses than foliar spraying. About 3.3% and 4.3% of plant genes showed statistically significant differential expressions because of foliar spray and root dipping treatments, respectively. The foliar spray treatment led to changes in two out of the five identified gene modules, comprised of 216 and 890 genes, respectively. Root dipping led to changes in 24 out of the 32 identified gene modules. Although both treatments led to increased grain yield in previous field studies, many of the induced plant response changes in terms of directional changes of differentially expressed genes differed between root dipping and foliar spraying, particularly those related to chloroplast activities. The large non‐overlapping induced plant changes between root dipping and foliar spraying explain the additive effects of the two treatments in increasing grain yield in previous field studies. The present results also suggest that reduction of blast because of foliar application of T. asperellum is unlikely because of direct antagonism against M. oryzae , but more likely via induced plant defence responses.