Some photosynthetic organisms live in extremely low light environments. Light limitation is associated with selective forces as well as reduced exposure to mutagens, and over evolutionary timescales it can leave a footprint on species' genomes. Here, we present the chloroplast genomes of four green algae (Bryopsidales, Ulvophyceae), including the endolithic (limestone-boring) alga Ostreobium quekettii, which is a low light specialist. We use phylogenetic models and comparative genomic tools to investigate whether the chloroplast genome of Ostreobium corresponds to our expectations of how low light would affect genome evolution. Ostreobium has the smallest and most gene-dense chloroplast genome among Ulvophyceae reported to date, matching our expectation that light limitation would impose resource constraints reflected in the chloroplast genome architecture. Rates of molecular evolution are significantly slower along the phylogenetic branch leading to Ostreobium, in agreement with the expected effects of low light and energy levels on molecular evolution. We expected the ability of Ostreobium to perform photosynthesis in very low light to be associated with positive selection in genes related to the photosynthetic machinery, but instead, we observed that these genes may be under stronger purifying selection. Besides shedding light on the genome dynamics associated with a low light lifestyle, this study helps to resolve the role of environmental factors in shaping the diversity of genome architectures observed in nature.