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BrlA and AbaA are key activators of the central developmental pathway (CDP) that controls asexual development in <i>Aspergillus</i> but their roles remain insufficiently understood in hypocerealean insect pathogens. Here, regulatory roles of BrlA and AbaA orthologs in <i>Metarhizium</i> <i>robertsii</i> (Clavicipitaceae) were characterized for comparison to those elucidated previously in <i>Beauveria bassiana</i> (Cordycipitaceae) at phenotypic and transcriptomic levels. Time-course transcription profiles of <i>brlA</i>, <i>abaA</i>, and the other CDP activator gene <i>wetA</i> revealed that they were not so sequentially activated in <i>M.</i> <i>robertsii</i> as learned in <i>Aspergillus</i>. Aerial conidiation essential for fungal infection and dispersal, submerged blastospore production mimicking yeast-like budding proliferation in insect hemocoel, and insect pathogenicity via cuticular penetration were all abolished as a consequence of <i>brlA</i> or <i>abaA</i> disruption, which had little impact on normal hyphal growth. The disruptants were severely compromised in virulence via cuticle-bypassing infection (intrahemocoel injection) and differentially impaired in cellular tolerance to oxidative and cell wall-perturbing stresses. The Δ<i>brlA</i> and Δ<i>abaA</i> mutant shad 255 and 233 dysregulated genes (up/down ratios: 52:203 and 101:122) respectively, including 108 genes co-dysregulated. These counts were small compared with 1513 and 2869 dysregulated genes (up/down ratios: 707:806 and 1513:1356) identified in Δ<i>brlA</i> and Δ<i>abaA</i> mutants of <i>B. bassiana</i>. Results revealed not only conserved roles for BrlA and AbaA in asexual developmental control but also their indispensable roles in fungal adaptation to the insect-pathogenic lifecycle and host habitats. Intriguingly, BrlA- or AbaA-controlled gene expression networks are largely different between the two insect pathogens, in which similar phenotypes were compromised in the absence of either <i>brlA</i> or <i>abaA</i>.