The use of endophytic entomopathogenic fungi (EEF) represents a promising strategy to boost plant resistance in crops against both biotic and environmental stresses. However, the mechanisms by which this inoculation influences constitutive and herbivore-induced defenses to protect plants against pest insects remain unclear. To address this gap, we investigated whether the inoculation of the EEF Metarhizium robertsii can modulate sugarcane plant defenses and their resistance against the sugarcane borer Diatraea saccharalis. Specifically, we examined the endogenous levels of jasmonic acid (JA) and salicylic acid (SA), as well as the volatile emissions in sugarcane, in the absence and presence of infestation caused by D. saccharalis. We also explored how these inoculations might affect the oviposition preference of D. saccharalis (direct defense) and the chemotaxis of its main natural enemy, the parasitoid Cotesia flavipes (indirect defense), commonly used in biological control programs. Our findings revealed that M. robertsii inoculation alters sugarcane plant chemical traits, affecting their resistance differently against D. saccharalis infestation. In non-infested plants, the inoculation of M. robertsii increased JA and SA phytohormones, suppressed volatile emissions, and reduced egg-laying by D. saccharalis, while exhibiting no effect on C. flavipes attraction. Conversely, in D. saccharalis-infested plants, M. robertsii increased JA content and reduced SA levels, resulting in quantitatively different volatile emissions. These changes increased attraction of C. flavipes compared to infested plants without fungal inoculation. Our results demonstrate that M. robertsii inoculations can enhance sugarcane plants' constitutive defenses against D. saccharalis while improving their herbivore-induced indirect defenses in sugarcane.