This study delves into the compatible use of a parasitoid with multifunctional endophytic Entomopathogenic Ascomycetes (EA) in IPM under greenhouse conditions. The parasitoid Hyposoter didymator was evaluated against Spodoptera littoralis in a multitrophic system with melon plants that were endophytically colonized by one of three EA strains (Metarhizium brunneum [one] or Beauveria bassiana [two]). In the first scenario, plants were inoculated by three different methods, and after infestation with noctuid larvae, the parasitoid was released at a 1:20 ratio. Microbiological and molecular techniques allowed the identification of progressive colonization throughout the whole plant life cycle, and for B. bassiana, approximately 20% of seeds from new fruits were colonized. The parasitoid was shown to be compatible with all strains and application methods, with total mortality rates ranging from 11.1 to 77.8%. Significant lethal and sublethal effects, a decrease in pupal weight and mortality of pupae showing abnormalities and an extension of the immature developmental times were observed for different strain–application method combinations. Additionally, the fungal treatments improved crop growth, as revealed by the significant gains in plant weight. In a second scenario (by inoculating plants with the fungi only by leaf spraying), and after infestation with noctuid larvae, the parasitoid was released at a 1:10 ratio, which revealed the remote fungal effect from the inoculation point and confirmed the compatibility of the parasitoid-EA-based strategy. These findings underscore the compatible use of a parasitoid with endophytic EA for S. littoralis control that can additionally exploit their multifunctionality for sustainable crop production.