Ecological theory postulates that the niche of co-occurring species must differ along some ecological dimensions in order to allow their stable coexistence. Yet, many biological systems challenge this competitive exclusion principle. For instance, insectivorous bats from the Northern Hemisphere typically form local assemblages of multiple species sharing highly similar functional traits and pertaining to identical feeding guilds. Although their trophic niche can be accessed with unprecedented details using genetic identification of prey, the underlying mechanisms of resource partitioning remain vastly unexplored. Here, we studied the differential diet of three phenotypically and phylogenetically closely-related bat species of the genus Plecotus in an area of sympatry and throughout their entire breeding season (April-October) using DNA metabarcoding. Even at such a small geographic scale, we identified strong seasonal and spatial variation of their trophic niche at both intra- and inter-specific levels. Indeed, while the different bats fed on a distinct array of prey during spring, they showed higher niche overlap during summer and fall, when all three bat species switched their hunting behavior to feed on few temporarily abundant moths. Furthermore, by considering the ecological traits of prey species, we inferred from the menu of each bat species that feeding grounds and hunting techniques differed suggesting that niche partitioning was primarily habitat-driven. As predicted by their phylogenetic relationships, the two most-closely related bat species exhibited the most distinct foraging habitat preferences, while the third, more distantly-related species was more generalist. These results highlight the need of extensive samples to fully understand species coexistence.