Bacterial ABC toxins are virulence factors expressed by a number of insect and mammalian pathogens. They are secreted tripartite pore-forming complexes (>2 MDa in size) that perforate the insect midgut cell membrane and deliver a lethal cytotoxin. Some members of the Photorhabdus & Xenorhabdus genera are nematode-associated pathogens while species of the Serratia & Yersinia genera are direct pathogens of insects. We have investigated the structure and target specificity of YenTc, an orally available ABC toxin expressed by Yersinia entomophaga, a pathogen of the New Zealand grass grub and have determined structure of the pre-pore and pore-form of YenTc. These structures revealed an overall topology of the A subunit that is reminiscent of the previously characterised ABC toxin PTC3 from Photorhabdus luminescens, despite a lack of detectable amino acid sequence similarity in some key regions of the structure. A comparative analysis of the structures further suggest there may be some differences in the membrane targeting and host specificity mechanisms, distinguishing these toxins. In particular, YenTc and PTC3 reveal striking differences in the regions of their structures previously implicated in cell surface receptor binding. We identified novel domains which we term the “leg & feet” domains that, on the basis of current structural evidence, appear likely to be involved in regulating cell surface recognition either directly or via recruitment of additional receptor-binding subunits. While these findings shed light on the cytotoxic mechanism of action of YenTc, intriguing questions remain open, a better understanding of which could aid in the development and engineering of ABC toxins for biotechnological purposes.