Fine-scale genetic diversity and contemporary evolution can theoretically influence ecological dynamics in the wild. Such eco-evolutionary effects might be particularly relevant to the persistence of populations facing acute or chronic environmental change. However, experimental data on wild populations is currently lacking to support this notion. One way that ongoing evolution might influence the dynamics of threatened populations is through the role that selection plays in mediating the ‘rescue effect’, the ability of migrants to contribute to the recovery of populations facing local disturbance and decline. Here, we combine experiments with natural catastrophic events to show that ongoing evolution is a major determinant of migrant contributions to population recovery in Trinidadian guppies (Poecilia reticulata). These eco-evolutionary limits on migrant contributions appear to be mediated by the reinforcing effects of natural and sexual selection against migrants, despite the close geographic proximity of migrant sources. These findings show that ongoing adaptive evolution can be a double-edged sword for population persistence, maintaining local fitness at a cost to demographic risk. Our study further serves as a potent reminder that significant evolutionary and eco-evolutionary dynamics might be at play even where the phenotypic status quo is largely maintained generation to generation.