Entomopathogenic nematodes (EPNs) are a guild of obligate insect parasites which share many physiological and behavioural traits with mammalian strongylid and strongyloidid parasites; including host-finding nictation behaviour. EPNs are also interesting from the perspective of insect biocontrol. Like other parasitic nematodes, EPNs employ a sophisticated chemosensory apparatus to detect potential hosts and communicate with conspecifics. Understanding the underlying molecular basis of relevant host-finding behaviours could facilitate improved EPN biocontrol approaches, and could lend insight to similar behaviours in economically important animal parasites. FMRFamide-like peptides are enriched and conserved across the Phylum Nematoda, and have been linked with motor and sensory function, including dispersal and aggregating behaviours in the free living nematode Caenorhabditis elegans. RNA interference (RNAi) was used to knockdown the expression of the FMRFamide-like protein 21 (GLGPRPLRFamide) gene (flp-21) in Steinernema carpocapsae infective juveniles (IJs). Our data show that S. carpocapsae is sensitive to neuronal RNAi, and that knockdown of flp-21 has a significant impact on dispersal, nictation and jumping behaviours. Immunocytochemical localisation of FLP-21 to paired anterior neurons corroborates the RNAi data, further suggesting a role in sensory modulation. This study represents the first demonstration of a functional RNAi pathway in S. carpocapsae, through which we have linked a single gene product to the coordination of nematode jumping, nictation, and dispersal behaviours in IJs. These data can underpin efforts to study these behaviours in other economically important parasites, and could facilitate molecular approaches to EPN strain improvement for biocontrol.