Polyploidy (whole genome duplication) is a ubiquitous feature of flowering plants that produces pronounced effects on phenotype, yet the underlying genetic mechanisms for these effects are mostly unknown. Photosynthesis is one of the most striking examples of how polyploids can differ dramatically from their diploid progenitors. We utilized the recurrent history of genome duplication within the genus Glycine to characterize the genetic and genomic mechanisms through which polyploidy impacts photosynthesis. Using genomic resources for the cultivated soybean (G. max), we examined how photosynthetic gene families have been shaped by ancient polyploidy events, as well as by non-polyploid (e.g., tandem) duplications, and found fundamental differences in the patterns of retention and loss for gene families encoding subunits of photosystems I and II compared to the Calvin cycle. We further showed that equivalent patterns emerge in two other paleopolyploids, Medicago truncatula and Arabidopsis thaliana. These differences suggest that photosystem gene families are dosage sensitive, whereas Calvin cycle gene families are not. We then devised an assay to quantify whole transcriptome size, as well as the expression of individual genes on a per-cell basis, enabling quantification of gene dosage responses and facilitating comparisons of gene expression across ploidy levels. Using this assay we demonstrated that the transcriptome of a recently formed Glycine allotetraploid (G. dolichocarpa) is ca. 1.4-fold larger than those of its diploid progenitors (G. tomentella and G. syndetika), and that most genes exhibit partial dosage compensation in the tetraploid. Because polyploidy is associated with enhanced stress tolerances, we also examined the effects of polyploidy on nonphotochemical quenching (NPQ), a set of mechanisms to protect the photosynthetic machinery under excess light stress. We showed that the G. dolichocarpa tetraploid has enhanced NPQ capacity under excess light compared to its diploid progenitors. Transcript profiling revealed that the tetraploid over-expresses two classes of galactolipid synthase genes, which results in altered leaf lipid profiles that may explain the differences in NPQ.