Summary1. Plants and their herbivores may influence each other's fitness and, hence, genetic dynamics, as well as their demography. Conversely, variation in fitness-related traits may influence the occurrence or intensity of the interaction. Disentangling the fitness consequences of an interaction in nature from the influence of fitness variation on it is challenging, but important to clarifying the ecological and evolutionary dynamics of plants with their herbivores. 2. As part of a larger effort to elucidate eco-evolutionary dynamics in a population of Echinacea angustifolia that is subject to severe fragmentation, we initiated an experiment in 2001 to evaluate differences in fitness among plants of three genotypic classes resulting from matings of plants from different remnant populations ('between', B), plants randomly chosen from the same remnant ('within', W) and maternal siblings ('inbreds', I). The experiment was planted into a field undergoing restoration to a prairie community. Fitness components of individual plants were recorded through 2012. During 2004-2010, each plant was also monitored for its load of Aphis echinaceae, a specialist insect herbivore. 3. Within a season, aphid-load depended consistently on a plant's location and on its load the previous season. Further, flowering individuals generally harboured more aphids than non-flowering plants. In analyses of overall plant fitness, within each genotypic class, fitness was greatest for plants with the greatest aphid-loads, consistent with the preference of aphids for flowering individuals. Inbreeding depression was severe, with I plants producing 60% fewer achenes than W or B plants, and varied with aphid-load. To distinguish the role of aphid choice from the effect of aphid herbivory in the relationship between plant fitness and aphid-load, we evaluated how components of fitness varied with prior aphid-load. Notably, genotype I plants with high aphid-loads the previous year produced far fewer achenes per flower head than those that carried fewer aphids. 4. Synthesis. Sibmating reduces individuals' demographic contribution by 60% over the first 12 years. Outbred individuals tolerate this aphid; each produces on average about 200 achenes per head in a year, despite a heavy aphid-load the previous year. However, inbreeding, which is greater in severely fragmented prairie habitat, results in poor tolerance. Aphid herbivory exacerbates inbreeding depression, further reducing the contribution of those individuals to population growth. This study illustrates an approach that helps to distinguish fitness-dependent attraction of herbivores from the effects of herbivory on plant fitness and demography, a goal that is critically important to eco-evolutionary understanding.