Remarkable advances in developmental genetics in the past two decades allow us to approach the evolution of animal design by elucidating the molecular mechanisms underlying divergent body plans. The ancestry and evolution of segmented body plans in the bilaterians has been an active area of investigation in this field of study. Although segmentation mechanisms have been extensively studied for the fruit fly Drosophila melanogaster, Drosophila exhibits an evolutionarily derived mode of development, and molecular mechanisms underlying Drosophila segmentation may be unrepresentative for arthropods, even for insects. We have been studying the developmental system of the cricket, Gryllus bimaculatus, to understand more ancestral and general segmentation mechanisms for insects than those of Drosophila. In Gryllus, anterior segments are specified almost simultaneously, whereas posterior segments are specified sequentially in the extending posterior region. This mode of segmentation is general and probably ancestral for arthropods. Our RNA interference-based analyses of the functions and regulatory interactions of Gryllus orthologues of Drosophila segmentation genes have revealed surprisingly divergent aspects of the segmentation system in Gryllus in comparison with that of Drosophila. For example, the anteroposterior patterning in Gryllus is principally controlled by the caudal (cad) gene, probably without bicoid, unlike Drosophila. Comparisons of regulatory networks of segmentation genes between Gryllus and Drosophila suggest that regulatory interactions between the genes vary among insects, despite conservation of the network component genes. This implies that the molecular mechanisms of segmentation have changed dynamically during insect evolution, whereas the segmented body plan itself has been conserved. We also discuss evolution of developmental systems generating segment patterns in non-arthropod bilaterian animals.