In plants and algae, photosynthesis is driven by the absorption of sunlight energy by networks of pigments housed within light-harvesting proteins. Special photosynthetic complexes can intercept the low-energy photons corresponding to the far-red spectrum of the photosynthetically active radiation. These so-called red chlorophyll forms are found in multiple lineages of the Viridiplantae clade, are formed upon a change in spatial organization of chromophores within specific subunits of the photosystem I supercomplex, and can be detected by their unique red-shifted fluorescence emission signatures. Red forms enabled phototrophs to colonize light-limited ecological niches, especially where far-red radiation is enriched by leaf shading. The protein environment plays a key role in determining the occurrence of red forms, promoting strong excitonic interactions among chlorophyll a molecules and facilitating their excitation by low-energy photons. In this review, we present a comprehensive account of the evolutionary diversity of long-wavelength-driven photosynthesis in eukaryotes, and detail the biophysical and structural determinants of this phenomenon. Finally, we discuss how this knowledge can be applied in biotechnology to engineer crop canopies with broadened light absorption and higher yield potential.