The regulation of virulence in plant-pathogenic fungi has emerged as a key area of importance underlying host infections. Pf2 is a member of the Zn₂-Cys₆ family of fungal transcription factors (TFs), where orthologues regulate the expression of genes linked to parasitism in several plant-pathogen lineages. These include PnPf2 which controls the expression of necrotrophic effector (NE) genes in Parastagonospora nodorum, the causal agent of septoria nodorum blotch of wheat. As a result, regulation exerted by PnPf2 dictates the outcome of effector-triggered susceptibility on wheat, wheat. However, direct genomic targets and whether other are regulators involved in NE gene regulation, remain unknown. We used chromatin immuno-precipitation (ChIP-seq) and a mutagenesis analysis to investigate these components. Two distinct binding motifs connected to positive gene-regulation were characterised and genes directly targeted by PnPf2 were identified. These included genes encoding major effectors and other components associated with the P. nodorum pathogenic lifestyle, such as carbohydrate-active enzymes and nutrient assimilators. This supports a direct involvement of PnPf2 in coordinating virulence on wheat. Other TFs were also prominent PnPf2 targets, suggesting it also operates within a transcriptional network. Several TFs were therefore functionally investigated in connection to fungal virulence. Distinct metabolic and developmental roles were evident for the newly characterised Pro1, Ada1, Ebr1 and the carbon-catabolite repressor CreA. Overall, the results uphold PnPf2 as the central transcriptional regulator orchestrating genes that contribute to virulence on wheat and provide mechanistic insight into how this occurs