Sap-sucking hemipterans host specialized, heritable microorganisms that supplement their unbalanced diet with essential nutrients. These microbes show unusual features that provide a unique perspective on the evolution of life but have not been systematically studied. Here, we combine microscopy with high-throughput sequencing to revisit 80-year-old reports on the diversity of symbiont transmission modes in a broadly distributed planthopper family Dictyopharidae. We show that in all species examined, the ancestral nutritional endosymbionts Sulcia and Vidania are complemented by co-primary symbionts, either Arsenophonus or Sodalis, acquired several times independently by different host lineages. Like in other obligate sap-feeders, the ancestral symbionts produce essential amino acids, whereas co-primary symbionts contribute to the biosynthesis of B vitamins. These symbionts reside within separate bacteriomes within the abdominal cavity, although in females, Vidania also occupies bacteriocytes in the rectal organ. Notably, the symbionts are transmitted from mothers to offspring in two alternative ways. In most examined species, all nutritional symbionts simultaneously infect the posterior end of the full-grown (vitellogenic) oocytes and next gather in their perivitelline space. In contrast, in other species, Sodalis colonizes the cytoplasm of the anterior pole of young (previtellogenic) oocytes forming a cluster separate from the "symbiont ball" formed by late-invading Sulcia and Vidania. Our data add to the evidence on frequent replacements of gammaproteobacterial symbionts combined with the relative functional stability of the nutritional functions during the evolution of sap-feeding insects, and show how newly-arriving microbes may utilize different strategies to establish long-term heritable symbiosis.