Flowering plants do not occur alone and often grow in mixed-species communities where pollinator sharing is high and interactions via pollinators can occur at pre- and post-pollination stages. While the causes and consequences of pre-pollination interactions have been well studied little is known about post-pollination interactions via heterospecific pollen (HP) receipt, and even less about the evolutionary implications of these interactions. In particular, the degree to which plants can evolve tolerance mechanisms to the negative effects of HP receipt has received little attention. Here, we aim to fill this gap in our understanding of post-pollination interactions by experimentally testing whether two co-flowering Clarkia species can evolve HP tolerance, and whether tolerance to specific HP ‘genotypes’ (fine-scale local adaptation to HP) occurs. We find that Clarkia species vary in their tolerance to HP effects. Furthermore, conspecific pollen performance and the magnitude of HP effects were related to the recipient's history of exposure to HP in C. xantiana but not in C. speciosa. Specifically, better conspecific pollen performance and smaller HP effects were observed in populations of C. xantiana plants with previous exposure to HP compared to populations without such exposure. These results suggest that plants may have the potential to evolve tolerance mechanisms to HP effects but that these may occur not from the female (stigma, style) but from the male (pollen) perspective, a possibility that is often overlooked. We find no evidence for fine-scale local adaptation to HP receipt. Studies that evaluate the adaptive potential of plants to the negative effects of HP receipt are an important first step in understanding the evolutionary consequences of plant–plant post-pollination interactions. Such knowledge is in turn crucial for deciphering the role of plant–pollinator interactions in driving floral evolution and the composition of co-flowering communities.