Significance Symbiosis between single-celled hosts and microalgae is a widespread and ecologically important phenomenon in oceanic plankton. Investigating such relationships can increase understanding of how novel organelles are acquired. Here, we integrate multiple subcellular approaches to show how a unicellular host manipulates the bioenergetic machinery of its algal endosymbionts and maximizes organic carbon production for its own benefit. Symbionts are blocked from dividing, but their photosynthetic machinery and associated mitochondrial network dramatically expand while keeping close physical proximity to each other. Genes involved in photosynthesis and carbon fixation are up-regulated, while those for carbon storage are down-regulated. Such extreme remodeling of microalgae has not been reported in other photosymbioses and provides insight into the putative early steps of plastid acquisition.