Ergosterols are essential components of fungal plasma membranes. Inhibitors targeting ergosterol biosynthesis (ERG) genes are critical for controlling fungal pathogens, including Magnaporthe oryzae, the fungus that causes rice blast. In this study we show that the Trm6/Trm61 complex catalyzes dynamic N1-methyladenosine at position 58 (m1A58) in 51 tRNAs of M. oryzae, significantly influencing translation at both initiation and elongation stages. The absence of m1A58 leads to substantial decreases in the translation of ERG genes, ergosterol production, and consequently, fungal virulence. Strikingly, simultaneously targeting the Trm6/Trm61 complex and the ergosterol biosynthesis pathway markedly improves control against rice blast. Our findings demonstrate the pivotal role of m1A58-mediated translational regulation in ergosterol production and fungal infection, offering a new strategy for fungicide development. Mass spectrometry data used in this paper are included in these uploaded files.