Irises in the section Oncocyclus (Siems.) Baker (Iris: Iridaceae) grow throughout the Middle East and have large and dark‐coloured flowers but no nectar reward available to flower visitors. Consequently, no reward‐collecting pollinators have been observed visiting the flowers during daytime. The only visitors are solitary male bees (Eucera spp.: Apidae) that enter the flowers at dusk and stay there overnight. Here we describe the mating system of Oncocyclus irises, and the role of night‐sheltering male bees in their pollination system. Pollen viability in I. haynei on Mt. Gilboa was very high (> 90 %) throughout all floral life stages. Stigmas were receptive in buds and in open flowers, but not in older ones. Self‐pollination yielded no fruits in three species, confirming complete self‐incompatibility in Oncocyclus irises. On average, 1.9 flowers were visited by each male bee before it settled for the night in the last one. Moreover, Iris pollen was present on the dorsal side of 38.8 % of males caught sheltering in flower models mounted near an I. atrofusca population, indicating that pollen is transferred between flowers by night‐sheltering solitary male bees. We have surveyed 13 flowering populations of six Oncocyclus species for the presence of night‐sheltering male bees as well as for fruit set. We found a positive correlation, indicating that sexual reproduction in Oncocyclus irises is dependent on night‐sheltering solitary male bees. Based on their complete self‐incompatibility, the absence of nectar‐collecting visitors during the day, and the transfer of pollen grains by the night‐sheltering solitary male bees, we conclude that fertilization of Oncocyclus irises is totally dependent on pollination by night‐sheltering solitary male bees.