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Learning and other forms of phenotypic plasticity have been suggested to enhance population divergence. Mate preferences can develop by learning, and species recognition might not be entirely genetic. We present data on female mate preferences of the banded demoiselle (Calopteryx splendens) that suggest a role for learning in population divergence and species recognition. Populations of this species are either allopatric or sympatric with a phenotypically similar congener (C. virgo). These two species differ mainly in the amount of wing melanization in males, and wing patches thus mediate sexual isolation. In sympatry, sexually experienced females discriminate against large melanin wing patches in heterospecific males. In contrast, in allopatric populations within the same geographic region, females show positive ("open-ended") preferences for such large wing patches. Virgin C. splendens females do not discriminate against heterospecific males. Moreover, physical exposure experiments of such virgin females to con- or hetero-specific males significantly influences their subsequent mate preferences. Species recognition is thus not entirely genetic and it is partly influenced by interactions with mates. Learning causes pronounced population divergence in mate preferences between these weakly genetically differentiated populations, and results in a highly divergent pattern of species recognition at a small geographic scale.