Intracellular symbioses between bacteria and insects are numerous, and alter the ecology and evolution of host and symbiont alike. Long-term persistence results from either exploitation (e.g., reproductive manipulations) or mutually beneficial interactions (e.g., nutritional mutualisms). The endosymbiont Hamiltonella defensa, while not essential for growth or survival of healthy aphids, protects aphids from attack by parasitoid wasps. In this thesis, I have used a variety of sequenced-based techniques to illuminate the population and genome dynamics of H. defensa and to disentangle how these factors contribute to its ability to persist and protect its hosts.I characterized the phylogenetic relationships among H. defensa strains from aphids and a whitefly using a multilocus approach. Most loci evolve in a clonal manner, and one cluster of strains may have given rise to an obligate symbiosis. Some H. defensa strains were infected with the bacteriophage APSE, which encodes putative eukaryotic specific toxins and has been suggested to be involved in protecting aphids. I sequenced the toxin locus and the flanking regions from the APSE strains and found that although the phage genome backbone was highly conserved, strains contained non-orthologous toxin-cassettes. Sequenced cassettes contained one of three putative toxin families: Shiga toxin, cytolethal distending toxin, and YD-repeat toxins. A correlation was noted that of several genetically identical H. defensa strains, the one without phage APSE encoding the YD-repeat toxin failed to protect its aphid host. This APSE strain carrying the YD-repeat toxin has since been demonstrated to be essential for protection in several related H. defensastrains.To examine additional bacterial encoded loci that might facilitate the persistence in and protection of aphids by H. defensa, I sequenced the genome of one strain and obtained partial genomes of two additional strains. These genomes exhibit a streamlined metabolism, but are littered with mobile DNA and putative virulence factors. Horizontal gene transfer, recombination and rearrangements are common, and phage and plasmids have played an important role in resorting genes. Thus, although H. defensa benefits its host, its facultative lifestyle has resulted in a pattern of genome evolution associated with reproductive parasites rather than long-term mutualists.