Spiny pollen has evolved independently in multiple entomophilous lineages. Sexual selection may act on exine traits that facilitate male mating success by influencing the transfer of pollen from the anther to the body of the pollinator, while natural selection acts to increase pollen survival. We postulated that relative to sexual congeners, apomictic dandelions undergo relaxed selection on traits associated with male mating success. We explored sexual selection on exine traits by measuring the propensity for Taraxacum spp. pollen to attach to hairs of flower-visiting bumblebees (Bombus spp.) or flies (Diptera: Syrphidae and Muscoidea) and assessed natural selection by testing whether pollen traits defend against consumption. Pollen picked up by bumblebees exhibited a narrower subset of spine-spacing phenotypes, consistent with stabilizing selection. Flies picked up larger pollen from flowers than expected at random. Surveys of corbiculae (pollen basket) contents from foraging bumblebees and feces of flies showed that pollen grains consumed by both kinds of visitors are similar in spine characteristics and size to those produced by the donor. When bees visit inflorescences of apomictic T. officinale, they pick up pollen with spine-spacing phenotypes above the mean and shifted toward those of sexual T. ceratophorum. We demonstrate that traits under sexual selection during pollen pickup vary among pollinators, while natural selection for pollen defense is nil in T. ceratophorum. In hybrid zones between apomictic and sexual dandelions, pollen traits place apomictic donors at a dispersal disadvantage, potentially reinforcing reproductive isolation.