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Pollinator sharing often leads to receipt of heterospecific pollen (HP) along with conspecific pollen. As a result, flowering plants can accumulate diverse communities of HP on stigmas. While variation in HP diversity is an important selective force contributing to flowering plant fitness, evolution and community assembly, our understanding of the extent and drivers of heterogeneity of HP diversity is limited.In this study, we examined the species compositions and abundances of ~1000 HP communities across 59 co‐flowering plant species in three serpentine seep communities in California, USA. We evaluated the variation in HP diversity (γ diversity) across plant species in each seep and asked whether the variation in HP γ diversity was caused by variation in HP diversity within stigmas (α diversity) or HP compositional variation among stigmas (β diversity) due to the replacement of HP species (turnover) or their loss (nestedness) from one stigma to another. We further evaluated the potential drivers of variation in HP α and β diversity using phylogenetic structural equation models.We found that variation in HP γ diversity across plant species was driven strongly by differences among species in HP α diversity and to a lesser extent by HP β diversity. HP community turnover contributed more to HP β diversity than nestedness consistently across plant species and seeps, suggesting a general pattern of HP compositional heterogeneity from stigma to stigma. The phylogenetic structural equation models further revealed that floral traits (e.g., stigma area, stigma‐anther distance, stigma exposure) and floral abundance were key in determining HP α diversity by influencing HP abundance (load size), while floral traits and abundance showed variable impact on HP β diversity (turnover and nestedness). Pollination generalism contributed relatively less to HP‐α and β diversity.These findings disentangle the heterogeneity in HP diversity at different levels, which is essential for understanding the process underlying patterns of HP receipt in plant communities. That floral traits drive the heterogeneity in HP diversity points to additional avenues by which HP receipt may contribute to plant evolution. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]