Adherence of conidia to insect integument is crucial for initiation of fungal infection through cuticular penetration and was previously reported to rely upon the Metarhizium-type adhesin Mad1 rather than Mad2, another adhesin crucial for conidial adherence of Metarhizium anisopliae to plant root surface. Mad1 and Mad2 have since been considered to function in fungal insect pathogenesis and plant root colonization respectively. Here, three adhesins were characterized in Beauveria bassiana, including Adh1/Mad1, Adh2/Mad2, and Adh3 known as filamentous hemagglutinin/adhesin and virulence factor in animal-pathogenic bacteria. Among those, only Adh2 was found to play a substantial role in sustaining the fungal virulence and some phenotypes associated with biological control potential. Disruption of adh2 resulted in decreased conidial adherence to insect wing cuticle, attenuated virulence via normal cuticle infection or cuticle-bypassing infection (injection), reduced blastospore production in an insect hemolymph-mimicking broth, largely reduced conidiation capacity, impaired conidial quality indicative of lowered viability, hydrophobicity, and UV resistance, but no growth defects on rich and scant media under normal or stressful culture conditions. The main phenotypic changes correlated well with repressed expression of developmental activator genes required for aerial conidiation and submerged blastospore production and of key hydrophobin genes essential for hydrophobin synthesis and assembly into rodlet bundles of conidial coat crucial for conidial adherence. In contrast, either adh1 or adh3 disruption caused insignificant changes in all phenotypes examined. These findings offer novel insight into a significance of Adh2, but a dispensability of Adh1 or Adh3, for insect-pathogenic lifecycle of B. bassiana.