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The biotrophic fungus <i>Sporisorium reilianum</i> causes destructive head smut disease in maize (<i>Zea mays</i> L.). To explore the pathogenicity arsenal of this fungus, we tracked its transcriptome changes during infection of the maize seedling mesocotyls of two near-isogenic lines, HZ4 and HZ4R, differing solely in the disease resistance gene <i>ZmWAK</i>. Parasitic growth of <i>S. reilianum</i> resulted in thousands of differentially expressed genes (DEGs) compared with growth in axenic culture. The protein synthesis and energy metabolism of <i>S. reilianum</i> were predominantly enriched with down-regulated DEGs, consistent with the arrested hyphal growth observed following colonization. Nutrition-related metabolic processes were enriched with both up- and down-regulated DEGs, which, together with activated transmembrane transport, reflected a potential transition in nutrition uptake of <i>S. reilianum</i> once it invaded maize. Notably, genes encoding secreted proteins of <i>S. reilianum</i> were mostly up-regulated during biotrophy. <i>ZmWAK</i>-mediated resistance to head smut disease reduced the number of DEGs of <i>S. reilianum</i>, particularly those related to the secretome. These observations deepen our understanding of the mechanisms underlying <i>S. reilianum</i> pathogenicity and <i>ZmWAK</i>-induced innate immunity.