Two fundamental symbiosis‐based trophic types are recognized among Zoanthidea (Cnidaria, Anthozoa): fixed carbon is either obtained directly from zooxanthellae photosymbionts or from environmental sources through feeding with the assistance of host‐invertebrate behaviour and structure. Each trophic type is characteristic of the suborders of Zoanthidea and is associated with substantial distributional asymmetries: suborder Macrocnemina are symbionts of invertebrates and have global geographic and bathymetric distributions and suborder Brachycnemina are hosts of endosymbiotic zooxanthellae and are restricted to tropical photic zones. While exposure to solar radiation could explain the bathymetric asymmetry it does not explain the geographic asymmetry, nor is it clear why evolutionary transitions to the zooxanthellae‐free state have apparently occurred within Macrocnemina but not within Brachycnemina. To better understand the transitions between symbiosis‐based trophic types of Zoanthidea, a concatenated data set of nuclear and mitochondrial nucleotide sequences were used to test hypotheses of monophyly for groups defined by morphology and symbiosis, and to reconstruct the evolutionary transitions of morphological and symbiotic characters. The results indicate that the morphological characters that define Macrocnemina are plesiomorphic and the characters that define its subordinate taxa are homoplasious. Symbioses with invertebrates have ancient and recent transitions with a general pattern of stability in host associations through evolutionary time. The reduction in distribution of Zoanthidea is independent of the evolution of zooxanthellae symbiosis and consistent with hypotheses of the benefits of invertebrate symbioses, indicating that the ability to persist in most habitats may have been lost with the termination of symbioses with invertebrates.