Light is the most potent stimulus for synchronizing the endogenous circadian timing system to the 24 h day. The timing, intensity, duration, pattern and wavelength of light are known to modulate photic resetting of the circadian system and acute suppression of melatonin secretion. The effect of prior photic history on these processes, however, is not well understood. Although previous studies have shown that light history affects the suppression of melatonin in response to a subsequent light exposure, here we show for the first time that a very dim light history, as opposed to a typical indoor room illuminance, amplifies the phase-shifting response to a subsequent sub-saturating light stimulus by 60–70%. This greater efficacy provides evidence for dynamic adaptive changes in the sensitivity of circadian ocular photoreception. This plasticity has important implications for the optimization of light therapy for the treatment of circadian rhythm sleep disorders.