Marine cyanobacteria are responsible for ~25% of the fixed carbon that enters the ocean biosphere. It is thought that abundant co-occurring viruses play an important role in regulating population dynamics of cyanobacteria and thus the cycling of carbon in the oceans. Despite this, little is known about how viral infections 'play-out' in the environment, particularly whether infections are resource or energy limited. Photoautotrophic organisms represent an ideal model to test this since available energy is modulated by the incoming light intensity through photophosphorylation. Therefore, we exploited phototrophy of the environmentally relevant marine cyanobacterium Synechococcus and monitored growth of a cyanobacterial virus (cyanophage). We found that light intensity has a marked effect on cyanophage infection dynamics, but that this is not manifest by a change in DNA synthesis. Instead, cyanophage development appears energy limited for the synthesis of proteins required during late infection. We posit that acquisition of auxiliary metabolic genes (AMGs) involved in light-dependent photosynthetic reactions acts to overcome this limitation. We show that cyanophages actively modulate expression of these AMGs in response to light intensity and provide evidence that such regulation may be facilitated by a novel mechanism involving light-dependent splicing of a group I intron in a photosynthetic AMG. Altogether, our data offers a mechanistic link between diurnal changes in irradiance and observed community level responses in metabolism, i.e., through an irradiance-dependent, viral-induced release of dissolved organic matter (DOM).