Pantoea ananatis is a bacterium that is found in many agronomic crops and agricultural pests. Here, we isolated a P. ananatis strain (Lstr) from the rice planthopper Laodelphax striatellus, a notorious pest that feeds on rice plant sap and transmits rice viruses, in order to examine its genome and biology. P. ananatis Lstr is an insect symbiont that is pathogenic to the host insect and appears to mostly inhabit the gut. Its pathogenicity thus raises the possibility of using the Lstr strain as a biological agent. To this end, we analysed the genome of the Lstr strain and compared it with the genomes of other Pantoea species. Our analysis of these genomes shows that P. ananatis can be divided into two mono-phylogenetic clades (clades one and two). The Lstr strain belongs to clade two and is grouped with P. ananatis strains that were isolated from rice or rice-associated samples. A comparative genomic analysis shows that clade two differs from clade one in many genomic characteristics including genome structures, mobile elements, and categories of coding proteins. The genomes of clade two P . ananatis are significantly smaller, have much fewer coding sequences but more pseudogenes than those of clade one, suggesting that clade two species are at the early stage of genome reduction. On the other hand, P. ananatis has a type VI secretion system that is highly variable but cannot be separated by clades. These results clarify our understanding of P. ananatis ’ phylogenetic diversity and provide clues to the interactions between P. ananatis , host insect, and plant that may lead to advances in rice protection and pest control.