Single host–symbiont interactions should be reconsidered from Koch's postulates to the notion of a ‘pathobiome’. We revisit here the interactions between entomopathogenic nematodes (EPNs) and their microbiota. The isolation of the bacteria from the infective juveniles (IJs) of Steinernema and Heterorhabditis species systematically led to the identification of Xenorhabdus and Photorhabdus species, respectively, supporting the concept of a symbiotic relationship. In this ‘endosymbiotic bacterium-focused view’, the dogma of natural monoxenicity between the nematode and the endosymbiotic bacterium has become widely accepted as a rule in the scientific community. However, recent high-throughput sequencing studies have shown that EPNs are also associated with other bacterial communities, referred to here as the second bacterial circle of EPNs. Our team profiled the microbiota of Steinernema carpocapsae IJs. Multigenic metabarcoding (16S and rpoB markers) showed that the bacterial community associated with laboratory-reared IJs consisted of the core symbiont (Xenorhabdus nematophila) together with a frequently associated microbiota (FAM) consisting of about a dozen of Proteobacteria (Pseudomonas, Stenotrophomonas, Alcaligenes, Achromobacter, Pseudochrobactrum, Ochrobactrum, Brevundimonas, Deftia, etc.). We validated the profile of the Steinernema FAM by culturomic approaches, isolating diverse bacterial taxa. Within the FAM, two species, Pseudomonas protegens and P. chlororaphis, displayed entomopathogenic properties suggestive of a role in Steinernema virulence and membership of the Steinernema pathobiome. We also hypothesise a potential positive contribution of the second bacterial circle to the whole infectious process and to completion of the main phases of the EPN life cycle. The microbial communities of low complexity associated with EPNs will permit future microbiota manipulation experiments to decipher overall microbiota functioning in the infectious process triggered by EPN in insects and, more generally, in EPN ecology.