Discovery of novel secretome proteins contributes to the understanding of host-pathogen interactions. Here we report a rich diversity of secreted proteins from the interaction between grain aphids (host, insect order Hemiptera) and fungi of the order Entomophthorales (insect pathogens), made possible by screening a cDNA library constructed directly on field sampled material with an advanced method, unbiased of known sequences and/or functions. We show for the first time that fungi from the genera Pandora and Entomophthora are armed with a battery of hydrolytic enzymes for penetration of the host cuticle, enabling both access to the hemolymph and exit for sporulation. Further, they secrete enzymes, most notably a number of lipases, for digestion of easily accessible high-energy compounds within the hemolymph. In contrast, we identified only few host genes inferred to be involved in the interaction, indicating that aphids only respond weakly to the presence of the pathogens and supporting recent findings that aphids have a reduced immune repertoire.