Coral-dinoflagellate symbiosis underpins the evolutionary success of corals reefs. Successful exchange of molecules between the cnidarian host and the Symbiodiniaceae algae enables the mutualistic partnership. The algae translocate photosynthate to their host in exchange for nutrients and shelter. The photosynthate must traverse multiple membranes, most likely facilitated by transporters. Here, we compared gene expression profiles of free-living cultured and freshly isolated Breviolum minutum, the homologous symbiont of the coral model, the sea anemone Exaiptasia pallida. Additionally, we assessed expression levels of a select a list of candidate host transporters-of-interest in anemones with and without symbionts. Our transcriptome analyses highlight the distinctive nature of the two algal life stages, with many gene expression level changes correlating to the different morphologies, cell cycles, and metabolisms adopted in hospite versus free-living. Morphogenesis-related genes that likely underpin the metamorphosis process observed when symbionts enter a host cell were up-regulated. Conversely, many down-regulated genes appear to be indicative of the protective and confined nature of the symbiosome. Our results emphasize the significance of transmembrane transport to the symbiosis, and in particular of ammonium and sugar transport. Further, we pinpoint and characterize candidate transporters—localized variously to the algal plasma membrane, the host plasma membrane, and the symbiosome membrane— that likely serve pivotal roles in the interchange of material during symbiosis. Our study provides new insights that expand our understanding of the molecular exchanges that enable symbiotic relationship.