Bigelowiella natans is a marine chlorarachniophyte whose plastid was acquired secondarily via endosymbiosis with a green alga. During plastid evolution, the photosynthetic endosymbiont would have integrated with the host metabolic pathways. This would require the evolution and coordination of strategies to cope with changes in light intensity that includes changes in the expression of both endosymbiont and host-derived genes. To investigate the transcriptional response to light intensity in chlorarachniophytes, we conducted an RNA-seq experiment to identify differentially expressed genes following a 4-h shift to high or very-low light. A shift to high light altered the expression of over 2,000 genes, many involved with photosynthesis, PSII assembly, primary metabolism, and reactive-oxygen scavenging. These changes are an attempt to optimize photosynthesis and increase energy sinks for excess reductant, while minimizing photooxidative stress. A transfer to very-low light resulted in a lower photosynthetic performance and metabolic alteration, reflecting an energy-limited state. Genes located on the nucleomorph, the vestigial nucleus in the plastid, had few changes in expression in either light treatment, indicating this organelle has relinquished most transcriptional control to the nucleus. Overall, during plastid origin, both host and transferred endosymbiont genes evolved a harmonized transcriptional network to respond to a classic photosynthetic stress.