Entomopathogenic nematodes of the genera Steinernema and Heterorhabditis, along with their bacterial symbionts from the genera Xenorhabdus and Photorhabdus, respectively, are important biological control agents against agricultural pests. Rapid progress in the development of genomic tools has catalyzed a transformation of the systematics of these organisms, reshaping our understanding of their phylogenetic and cophlylogenetic relationships. In this review, we discuss the major historical events in the taxonomy and systematics of this group of organisms, highlighting the latest advancements in these fields. Additionally, we synthesize information on nematode–bacteria associations and assess the existing evidence regarding their cophylogenetic relationships.