The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including 'temperate-A', A(I), Phylotype A ' (A-prime) and 'Mediterranean A', is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized 'yellow cells' as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum and P. actiniarum, and describe six new species. Each symbiont species exhibits high host fidelity for particular species of sea anemone, soft coral, stony coral and a rhizostome jellyfish. Philozoon is most closely related to Symbiodinium (formerly Clade A), but, unlike its tropical counterpart, occurs in hosts in shallow temperate marine habitats in northern and southern hemispheres including the Mediterranean Sea, north-eastern Atlantic Ocean, eastern Australia, New Zealand and Chile. The existence of a species-diverse lineage adapted to cnidarian hosts living in high latitude habitats with inherently wide fluctuations in temperature calls further attention to the ecological and biogeographic reach of the Symbiodiniaceae. HIGHLIGHTS A dinoflagellate genus symbiotic with temperate invertebrates is characterized and named using a discarded taxonomic term revived from the golden age of Natural Historians. The work highlights how animal-algal mutualisms are evolved to thrive under a broad range of environmental conditions.