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In animal-pollinated plants, local adaptation to pollinator behaviour or morphology can restrict gene flow among plant populations; but gene flow may also prevent divergent adaptation. Here, we examine possible effects of gene flow on plant–pollinator trait matching in two varieties of Joshua tree (Agavaceae: Yucca brevifolia). The two varieties differ in strikingly in floral morphology, which matches differences in the morphology of their pollinators. However, this codivergence is not present at a smaller scale: within the two varieties of Joshua tree, variation in floral morphology between demes is not correlated with differences in moth morphology. We use population genetic data for Joshua tree and its pollinators to test the hypotheses that gene flow between Joshua tree populations is structured by pollinator specificity, and that gene flow within the divergent plant–pollinator associations ‘swamps’ fine-scale coadaptation. Our data show that Joshua tree populations are structured by pollinator association, but the two tree varieties are only weakly isolated – meaning that their phenotypic differences are maintained in the face of significant gene flow. Coalescent analysis of gene flow between the two Joshua tree types suggests that it may be shaped by asymmetric pollinator specificity, which has been observed in a narrow zone of sympatry. Finally, we find evidence suggesting that gene flow among Joshua tree sites may shape floral morphology within one plant–pollinator association, but not the other.