Ecological and evolutionary processes historically have been assumed to operate on significantly different time scales. We know now from theory and work in experimental and model systems that these processes can feed back on each other on mutually relevant time scales. Here, we present evidence of a soil-mediated eco-evolutionary feedback on the population dynamics of an invasive biennial plant, Alliaria petiolata. As populations age, natural selection drives down production of A. petiolata's important anti-mycorrhizal allelochemical, sinigrin. This occurs due to density dependent selection on sinigrin, which is favored under interspecific, but disfavored under intraspecific, competition. We show that population stochastic growth rates (λS) and plant densities are positively related to sinigrin concentration measured in seedling roots. This interaction is mediated by sinigrin's positive effect on seedling and summer survival, which are important drivers of λS. Together, these illustrate how the evolution of a trait shaped by natural selection can influence the ecology of a species over a period of just years to decades, altering its trajectory of population growth and interactions with the species in the soil and plant communities it invades. Our findings confirm predictions that eco-evolutionary feedbacks occur in natural populations. Furthermore, they improve our conceptual framework for projecting future population growth by linking variation in plant demography to a critical competitive trait (sinigrin) whose selective advantages decrease as populations age.