There is a complex interplay between the regulation of flagellar motility and the expression of virulence factors in many bacterial pathogens. Here, we review the literature on the direct and indirect roles of flagellar motility in mediating the tripartite interaction between entomopathogenic bacteria (Photorhabdus and Xenorhabdus), their nematode hosts, and their insect targets. First, we describe the swimming and swarming motility of insect pathogenic bacteria and its impact on insect colonization. Then, we describe the coupling between the expression of flagellar and virulence genes and the dynamic of expression of the flagellar regulon during invertebrate infection. We show that the flagellar type 3 secretion system (T3SS) is also an export apparatus for virulence proteins in X. nematophila. Finally, we demonstrate that phenotypic variation, a common property of the bacterial symbionts of nematodes, also alters flagellar motility in Photorhabdus and Xenorhabdus. Finally, the so-called phenotypic heterogeneity phenomenon in the flagellar gene expression network will be also discussed. As the main molecular studies were performed in X. nematophila, future perspectives for the study of the interplay between flagellum and invertebrate interactions in Photorhabdus will be discussed.