Acceleration of photoprotective non-photochemical quenching (NPQ) responses to changes in light intensity has been suggested as a strategy to enhance crop yield. Despite many key crops utilising C4 photosynthesis, our current understanding of NPQ overwhelmingly comes from C3 species. Using a series of experiments on three phylogenetically controlled C3 and C4 comparisons, we show that NPQ relaxation is faster in C4 species. Temporal analysis of NPQ relaxation in leaves infiltrated with inhibitors to block proton motive force formation or xanthophyll de-epoxidation showed that the faster relaxation observed in C4 species is driven by a greater contribution of energy-dependent quenching (qE) to overall NPQ. We show that the C4-associated enhancement of qE is linked to altered regulation of lumen pH in C4 species, reflecting increases in cyclic electron flow and membrane proton conductivity to meet the increased ATP demands of the C4 pathway. Indeed, in two of the three tested C4 species, NPQ relaxation became significantly slower and statistically indistinguishable from paired C3 species when ATP and NADPH consumption was suppressed by performing measurements in CO2-free air. Altogether, our results suggest that NPQ responses in C4 species may already be optimised to maintain high photosynthetic efficiency in the fluctuating light conditions typically found within C4 canopies. Given the intrinsically faster NPQ in C4 photosynthesis, further acceleration of NPQ may have limited scope to enhance crop photosynthetic efficiency.