Diaphorina citri is the vector of “Candidatus Liberibacter asiaticus” (CLas), a bacterium associated with the citrus disease known as Huanglongbing (HLB). Previous mitochondrial genome (i.e. mitogenome) population analyses revealed the prevalence of two major mitochondrial groups (MGs) of D. citri in China, separated by elevation gradients. We assessed the population diversity of D. citri from 54 major citrus-producing areas within 11 provinces/regions of China. Additionally, endosymbiont genomes were assembled for “Ca. Carsonella ruddii” (CaCr) and “Ca. Profftella armatura” (CaPa) from next-generation sequencing of 31 new Chinese samples. Most of the D. citri diversity came from single nucleotide polymorphisms (SNPs) within five mitochondrial genes: nad3, cox2, rrnL, cob, and atp6. Nine SNPs clustered the analyzed D. citri mitogenomes into three major MGs comprising seven subgroups. Independent phylogenetic trees were generated for the endosymbionts CaCr and CaPa, and a CaPa plasmid, supporting the patterns obtained for D. citri mitogenomes while adding complexity layers. Genomic data from CaCr, CaPa, along with the plasmids from CaPa contribute to the genetic diversity—consisting of 68 SNPs and two genomic gaps—reproducing phylogenetic structures outlined by previous mitochondrial genomic studies. Additionally, both the mitogenomes and the endosymbiont genomes revealed subgroups within the original MG clusters, based on further 154 SNPs and 17 gaps. Thus, the combined genomic approach reveals further aspects about population diversity and natural history of this invasive species. Further understanding of D. citri and its endosymbionts can, therefore, aid D. citri HLB management protocols and help forecast territorial expansion events.