Dinoflagellates of the family Symbiodiniaceae are best known as photosymbionts of corals, although their ancestor is believed to have been free-living. Among Symbiodiniaceae lineages, the early-diverging genus Effrenium with its sole species Effrenium voratum is exclusively free-living. The genome of E. voratum therefore likely retains ancestral features of family Symbiodiniaceae lost in other lineages due to genome streamlining resulting from symbiogenesis with corals and other marine hosts. To test this hypothesis, we generated de novo genome assemblies and transcriptomes for three isolates of E. voratum. Incorporating all available 19 Symbiodiniaceae genomes encompassing six genera in an alignment-free phylogenomic analysis, phylogenetic signal recovered from protein-coding genes support the established phylogeny of the family. In contrast, comparative analysis of non-coding and repetitive genomic regions suggests Effrenium diverged earlier than did Symbiodinium. Interestingly, E. voratum genes also exhibit features distinct from other Symbiodiniaceae: they have the highest GC-content (60%) in protein-coding regions, fewer pseudogenes, and two-fold longer introns. Our results in combination support the notion that these ancestral features were differentially impacted by symbiogenesis, thereby enabling hypothesis-driven research of the effects of co-evolution with various hosts on Symbiodiniaceae genomes.