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Heritable symbioses have been critical for the evolution of life. The genetic consequences of evolving a heritable symbiosis from the perspective of the symbiont are well established, but concomitant changes in the host remain unresolved. In stony corals, heritable, vertical transmission has evolved repeatedly, providing a unique opportunity to investigate the genomic basis of this complex trait. We conducted a comparative analysis of 25 coral transcriptomes to identify orthologous genes exhibiting signatures of positive selection and convergent amino acid substitutions in vertically transmitting lineages. The frequency of convergence events tends to be higher among vertically transmitting lineages, consistent with the proposed role of selection in driving the evolution of convergent transmission mode phenotypes. Of 10 774 orthologous genes, 403 exhibited at least one molecular convergence event and evidence of positive selection in at least one vertically transmitting lineage. Functional enrichments among these top candidate genes include processes previously implicated in symbiosis including endocytosis, immune response, cytoskeletal protein binding and cytoplasmic membrane-bounded vesicles. Finally, several novel candidates were identified among 100 genes showing evidence of positive selection at the particular convergence event, highlighting the value of our approach for generating new insight into host mechanisms associated with the evolution of heritable symbioses.