AbstractThe evolutionary success of sap-feeding hemipteran insects in the suborder Auchenorrhyncha was enabled by nutritional contributions from their heritable endosymbiotic bacteria. However, the symbiont diversity, functions, and evolutionary origins in this large insect group have not been broadly characterized using genomic tools. In particular, the origins and relationships among ancient betaproteobacterial symbiontsVidania(in Fulgoromorpha) andNasuia/Zinderia(in Cicadomorpha) are uncertain. Here, we characterized the genomes ofVidaniaandSulciafrom threePyropsplanthoppers (family Fulgoridae) to understand their metabolic functions and evolutionary histories. We find that, like in previously characterized planthoppers, these symbionts share nutritional responsibilities, withVidaniaproviding seven out of ten essential amino acids.Sulcialineages across the Auchenorrhyncha have a highly conserved genome but with multiple independent rearrangements occurring in an early ancestor of Cicadomorpha or Fulgoromorpha and in a few succeeding lineages. Genomic synteny was also observed within each of the betaproteobacterial symbiont generaNasuia,Zinderia,andVidania, but not across them, which challenges the expectation of a shared ancestry for these symbionts. The further comparison of other biological traits strongly suggests an independent origin ofVidaniaearly in the planthopper evolution and possibly ofNasuiaandZinderiain their respective host lineages. This hypothesis further links the potential acquisition of novel nutritional endosymbiont lineages with the emergence of auchenorrhynchan superfamilies.