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Significance Many organisms, from plants to humans, have long evolutionary histories with nematode worms. Historically these relationships have been assumed to be detrimental—as with intestinal or blood-borne parasites—or at best innocuous, to their hosts. However, this paradigm has been challenged recently, for example, with findings in mammals that worms can modulate their host’s immune system and thereby thwart autoimmune disease. In our study, we describe a phenomenon wherein sexually transmitted and parentally provided worms benefit their insect hosts, possibly by “engineering” the microbiome present in the maternally constructed chamber where offspring develop. Given nematodes’ association with many insects, particularly those with parental care, this phenomenon may be a more widespread feature of insect health., A recent accumulation of studies has demonstrated that nongenetic, maternally transmitted factors are often critical to the health and development of offspring and can therefore play a role in ecological and evolutionary processes. In particular, microorganisms such as bacteria have been championed as heritable, symbiotic partners capable of conferring fitness benefits to their hosts. At the same time, parents may also pass various nonmicrobial organisms to their offspring, yet the roles of such organisms in shaping the developmental environment of their hosts remain largely unexplored. Here, we show that the nematode Diplogastrellus monhysteroides is transgenerationally inherited and sexually transmitted by the dung beetle Onthophagus taurus. By manipulating artificial chambers in which beetle offspring develop, we demonstrate that the presence of D. monhysteroides nematodes enhances the growth of beetle offspring, empirically challenging the paradigm that nematodes are merely commensal or even detrimental to their insect hosts. Finally, our research presents a compelling mechanism whereby the nematodes influence the health of beetle larvae: D. monhysteroides nematodes engineer the bacterial and fungal communities that also inhabit the beetle developmental chambers, including specific taxa known to be involved in biomass degradation, possibly allowing larval beetles better access to their otherwise recalcitrant, plant-based diet. Thus, our findings illustrate that nongenetic inheritance can include intermediately sized organisms that live and proliferate in close association with, and in certain cases enhance, the development of their hosts’ offspring.