Some animal groups associate with the same vertically-transmitted microbial symbionts over extended periods of evolutionary time, punctuated by occasional symbiont switches to different microbial taxa. Here we test the oft-repeated suggestion that symbiont switches are linked with host diet changes, focusing on hemipteran insects of the suborder Auchenorrhyncha. These insects include the only animals that feed on plant xylem sap through the life cycle, as well as taxa that feed on phloem sap and plant parenchyma cells. Ancestral state reconstruction provides strong statistical support for a xylem-feeding auchenorrhynchan ancestor bearing the dual symbiosis with the primary symbiont Sulcia (Bacteroidetes) and companion symbiont “β-Sym” (β-proteobacteria). We identified 7 dietary transitions from xylem-feeding (six to phloem-feeding, one to parenchyma-feeding), but no reversions to xylem-feeding; five evolutionary losses of Sulcia, including replacements by yeast symbionts, exclusively in phloem/parenchyma-feeding lineages; and 14-15 losses of β-Sym, including 9 transitions to a different bacterial companion symbiont. Our analysis indicates that, although companion symbiont switching is not associated with shifts in host diet, Sulcia is likely required for xylem-feeding. Furthermore, the ancestral auchenorrhynchan bearing Sulcia and β-Sym likely represents the sole evolutionary origin of xylem feeding in the animal kingdom.