In regions where dinoflagellates dominate bioluminescent emissions, diurnal variations in bioluminescence potential (BPOT) can be influenced by both exogenous and endogenous factors. In summer 2009, measurements were made in the north-east Atlantic to examine the diurnal variations in BPOT in natural dinoflagellate communities and determine the influence of circadian regulation and light exposure. The maximum night BPOT was >23 times greater than the daytime levels for the same populations. Photosynthetic species were responsible for 55–75% of measured BPOT based on calculated light budgets. Under continual darkness, diurnal variability of BPOT was retained over a 48-h period, demonstrating a degree of circadian control. Results suggest that both photosynthetic and heterotrophic dinoflagellates exhibit circadian regulation of their bioluminescent capacity and light strongly influences the diurnal variation of BPOT. Circadian rhythms were photo-entrained to the phase of the natural photoperiod and light further inhibited daytime bioluminescence. Maximum night BPOT was significantly correlated with the previous day integrated photosynthetically active radiation (PAR) suggesting photo-enhancement within natural populations. A 21% decrease in integrated PAR was associated with a 26–29% decrease in maximum night BPOT for constant populations. Maximum night BPOT was damped by up to 73% when organisms were kept in constant darkness. Findings further quantify diurnal variations in BPOT in natural dinoflagellate populations and their relation to a number of taxonomic, cellular and environmental factors. Results emphasize the importance of considering the recent light history of bioluminescent communities when analysing or predicting in situ BPOT.