Interspecific pollen transfer (IPT), the pollen movement between plant species via shared pollinators, reduces the reproductive success of pollen-recipient plants due to hybridization with heterospecific pollen grains. As a result, IPT hinders coexistence of sympatric, co-flowering species by reducing their reproductive success. IPT likely exerts selective pressure on plant reproductive systems, particularly on sex allocation (resource investment to pollen versus ovules). However, the influence of IPT on the evolutionary dynamics of sex allocation and associated ecological processes remains poorly understood. Here, we explore how the female costs incurred by IPT affect the co-evolution and coexistence dynamics of two plant species. To address this, we construct a mathematical model capturing interactions between two plant species through pollen transfer and resource competition, and reduced fertilization caused by IPT. Our analysis focuses on a scenario where an invasive species with female-biased sex allocation enters a habitat occupied by a resident species with evolutionarily stable, equal sex allocation (Fisherian sex allocation). Using adaptive dynamics theory, we demonstrated that, irrespective of IPT strength, natural selection drives both species toward equal sex allocation, consistent with the Fisherian sex allocation theory. We present two key predictions of eco-evolutionary outcomes. First, when the impacts of IPT are comparable for both species, the resulting eco-evolutionary dynamics lead to their stable coexistence. In contrast, if IPT from the invasive species is disproportionately stronger than IPT from the resident species, the invasive species’ evolutionary shift from female-biased to equal sex allocation drives the resident species to extinction. Since local mate competition in small populations can favour female-biased sex allocation, our results suggest that invasive species experiencing reduced local mate competition may drive resident species to extinction. Our findings underscore the intricate role of IPT-driven sex allocation evolution in shaping coexistence of closely related plant species.