A survey on 148 clones of the aphid Rhopalosiphum padi from 11 widespread localities has been carried out to study the genetic structure of populations of this species as revealed by mitochondrial DNA restriction site and length polymorphisms as well as by restriction site analysis of a maternally inherited plasmid carried by the aphid eubacterial endosymbiont Buchnera aphidicola. Our results support the existence in the area under study of two main aphid maternal lineages strikingly coincidental with the two main reproductive categories displayed by this species. Those aphid clones possessing an incomplete life cycle that lacks the sexual phase (anholocyclic or androcyclic clones) show mitochondrial DNA (mtDNA) haplotype I and plasmid haplotype I, whereas those clones displaying the complete life cycle (holocyclic clones) posses some other distinct mtDNA haplotypes closely related to each other and plasmid haplotype II. While restriction-site analysis of maternally inherited markers points to a relatively ancient origin of anholocycly/androcycly (between 460 000 and 1 400 000 years) followed by interrupted gene flow with respect to the ancestral holocyclic population, mtDNA size variation also suggests that historical stochastic processes have a different effect on the evolution of both main aphid lineages. Evidence of occasional nuclear gene flow between lineages and its consequences on the correspondence between maternally inherited haplotypes and life cycle are also presented and discussed.