Heterospecific pollen transfer, the transfer of pollen between species, is common among co-flowering plants, yet the amount of pollen received is extremely variable among species. Intraspecific variation in heterospecific pollen receipt can be even greater, but we lack an understanding of its causes and fitness consequences in wild populations. We examined potential drivers of variation in heterospecific pollen receipt in Oenothera fruticosa. We evaluated the relationship between heterospecific and conspecific pollen receipt and considered how visitation by different pollinator groups, local floral neighborhood composition, and flowering phenology affect the total amount and proportion of heterospecific pollen received. Finally, we tested whether variation in heterospecific pollen receipt translated into lower seed production. Heterospecific pollen is ubiquitous on O. fruticosa stigmas, but the amount received is highly variable and unrelated to conspecific pollen receipt. Heterospecific pollen receipt depends on pollinator type, the proportion of nearby conspecific flowers, and flowering date. Significant interactions reveal that the effects of pollinator type and neighborhood are not independent, further contributing to variation in heterospecific pollen. Naturally occurring levels of heterospecific pollen were sufficient to negatively impact seed set, but large amounts of conspecific pollen counteracted this detrimental effect. Although selection could act on floral traits that attract quality pollinators and promote synchronous flowering in O. fruticosa, the risk of heterospecific pollen is equally dependent on local floral context. This work highlights how extrinsic and intrinsic factors contribute to intraspecific variation in heterospecific pollen receipt in wild plants, with significant fitness consequences.