Hemipteran insects are well-known for their ancient associations with beneficial bacterial endosymbionts, particularly nutritional symbionts providing the host with essential nutrients such as amino acids or vitamins lacking from the host’s diet. Thereby, these primary endosymbionts enable the exploitation of nutrient-poor food sources such as plant sap or vertebrate blood. In turn, the strictly host-associated lifestyle strongly impacts the genome evolution of the endosymbionts, resulting in small and degraded genomes. Over time, even the essential nutritional functions can be compromised, leading to the complementation or replacement of an ancient endosymbiont by another, more functionally versatile, bacterium. Herein, we provide evidence for a dual primary endosymbiosis in several psyllid species. Using metagenome sequencing, we produced the complete genome sequences of both the primary endosymbiont ‘CandidatusCarsonella ruddii’ and an as yet uncharacterizedEnterobacteriaceaebacterium from four species of the genusCacopsylla. The latter represents a new psyllid-associated endosymbiont clade for which we propose the name ‘CandidatusPsyllophila symbiotica’. Fluorescentin situhybridisation confirmed the co-localization of both endosymbionts in the bacteriome. The metabolic repertoire ofPsyllophilais highly conserved across host species and complements the tryptophan biosynthesis pathway that is incomplete in the co-occurringCarsonella. Unlike co-primary endosymbionts in other insects, the genome ofPsyllophilais almost as small as the one ofCarsonella, indicating an ancient co-obligate endosymbiosis rather than a recent association to rescue a degrading primary endosymbiont.