Entomopathogenic nematodes (EPNs) are ubiquitous soil-thriving organisms that use chemical cues to seek and infect soil-dwelling arthropods, yielding various levels of biological control. Going beyond soil application, scientists and practitioners started exploring the option of applying EPNs onto the foliage of crops in attempts to manage leaf-dwelling insect pests as well. Despite some success, particularly with protective formulations, it remains uncertain whether EPNs could indeed survive the phyllospheric environment, and successfully control foliar insect pests. In this context, we tested the potential of commercially produced Steinernema feltiae and S. carpocapsae, two of the most commonly used EPNs in the field of biological control, in controlling Lepidopteran foliar pests of economic importance, i.e. Tuta absoluta and Spodoptera spp. caterpillars as models. We first tested the survival and efficacy of both EPN species against the Lepidopteran caterpillars when applied onto tomato, sweet pepper and lettuce leaves, under controlled conditions and in commercial greenhouse conditions, respectively. Subsequently, we explored the behavioural responses of the EPNs to environmental cues typically encountered in the phyllosphere, and analysed plant volatile organic compounds (VOCs). Our results show that both S. feltiae and S. carpocapsae successfully survived and infected the foliar caterpillars, reaching similar level of control to a standard chemical pesticide in commercial practices. Remarkably, both EPN species survived and remained effective up to four days in the phyllosphere, and needed only a few hours to successfully penetrate the caterpillars. Interestingly, S. feltiae was attracted to VOCs from tomato plants, and tended to prefer those from caterpillar-induced plants, suggesting that the nematodes may actively forage toward its host, although it has never been exposed to leaf-borne volatiles during its evolution. The present study shows the high potential of steinernematids in managing major foliar pests in greenhouses and in becoming a key player in foliar biological control. In particular, the discovery that EPNs use foliar VOCs to locate caterpillar hosts opens up new opportunities in terms of application techniques and affordable effective doses.