Photosynthesis is a hallmark of plants, yet photosynthetic ability has been lost repeatedly through evolution, for example in the angiosperm genus Cuscuta. Genomic and ultrastructure studies suggest that Cuscuta species exhibit varying degrees of plastid functionality and consequent ability for photosynthesis. However, few direct physiological studies exist, and none that span multiple developmental stages of autotrophic, mixotrophic, and non-photosynthetic species in a phylogenetic framework. We paired photosynthetic efficiency measurements from imaging pulse amplitude modulated (Imaging-PAM) fluorometry with quantitative analysis of chlorophylls and carotenoids from six developmental stages from seedling through developing seed, and fourteen species representing both hemi- and holo-parasites in three of the four subgenera of Cuscuta, and the closely related autotroph Ipomoea. These data were compared using nonparametric hypothesis tests and Bayesian model testing in a phylogenetic framework. Overall, chlorophyll and carotenoid content, and photosynthetic efficiency was highest in meristematic regions such as shoot tips and developing seeds versus older stems or haustoria. Neoxanthin production, highly conserved in plants, was most likely lost once in Cuscuta, but then subsequently re-gained. Finally, complex relationships between photosynthetic efficiency and lutein epoxide concentration suggest differing roles of this compound in developmental stages that have high and low energetic needs. Thus, we conclude that photosynthesis is not “vestigial” in hemiparasitic plants such as Cuscuta, but rather is modulated based on developmental stage, and across the phylogeny.