Non-random dispersal can promote regional coexistence despite local priority effects and negligible immigration. In the many cases of animal-mediated dispersal, hitchhikers can coexist regionally when animal vectors respond to environmental cues. However, this possibility has been poorly understood, particularly when local priority effects lead to history-dependent exclusion. We used a mathematical model of competitive communities of nectar microbes in sticky monkeyflower (Diplacus aurantiacus) to study how feedbacks between microbial communities and pollinator-mediated dispersal affect coexistence. Analysis of this model suggests that regional coexistence occurs only when microbial communities influence pollinator visit frequency. This microbe–pollinator feedback creates positive density-dependence at the plant scale that results in spatial niche partitioning across multiple plants. This partitioning facilitates mutual invasibility and stable regional coexistence of microbes. Our results highlight the importance of interactions between dispersal and community composition across scales in shaping patterns of species coexistence (Nell et al. in prep.; preprint).