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Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these, <i>Cladocopium goreaui</i> is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of <i>C. goreaui</i> combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the <i>C. goreaui</i> genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions; 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in <i>C. goreaui</i>, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically diverse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of <i>C. goreaui</i> genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35–36% have putatively originated via horizontal gene transfer (HGT), predominantly (19–23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10–11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.