Microbial eukaryotes (protists) are important contributors to marine biogeochemistry and play essential roles as both producers and consumers in marine ecosystems. Among protists, mixotrophs—those that use both heterotrophy and autotrophy to satisfy their energy requirements—are especially important to primary production in oligotrophic regions where nutrient availability is otherwise limiting. For instance, acantharians accomplish mixotrophy by hosting Phaeocystis spp. as endosymbionts. Despite their ecological importance, Acantharea-Phaeocystis symbioses are understudied due to host fragility and inability to survive in culture. We investigated the evolution and ecological functioning of these symbioses by sequencing single-cell transcriptomes from sixteen acantharians. Since hosts harbor multiple Phaeocystis species, we prepared transcriptomes for the two most common symbiont species available in culture—P. cordata and P. jahnii—and evaluated differential gene expression between symbiotic and free-living cells. Results indicate photosynthesis genes are upregulated in symbiosis for both symbiont species, suggesting symbionts are photosynthesizing at elevated rates within hosts. However, biosynthesis and metabolism of storage carbohydrates and lipids are downregulated in symbiosis, indicating that extra energy captured through elevated photosynthesis is not retained. Symbiont gene expression suggests symbionts relinquish fixed carbon as small organonitrogen compounds, such as amides and amino acids, while receiving host-supplied nitrogen as urea and ammonium. Importantly, genes associated with protein kinase signaling pathways that promote cell proliferation are deactivated in symbionts. Manipulation of these pathways may prevent symbionts from overgrowing hosts and therefore represents a key component of maintaining the symbiosis. This study illuminates mechanisms of host control and nutrient transfer in an important microbial symbiosis in oligotrophic waters.