This article explores the combined evolutionary and ecological responses of resource uptake abilities in a generalist consumer to exploitative competition for one resource using a simple 2-resource model. It compares the sizes of ecologically and evolutionarily caused changes in population densities in cases where the original consumer has a strong or a weak trade-off in its abilities to consume the two resources. The analysis also compares the responses of the original species to competition when the competitor’s population size is or is not limited by the shared resource. While divergence in resource use traits in the resident generalist consumer is expected under all scenarios when resources are substitutable, the changes in population densities of the resources and resident consumer frequently differ between scenarios. The population of the original consumer often decreases as a result of its own adaptive divergence, and this decrease is often much greater than the initial ecological decrease. If the evolving consumer has a strong trade-off, the overlapped resource increases in equilibrium population density in response to being consumed by a generalist competitor. Some of these predictions differ qualitatively in alternative scenarios involving sustained variation in population densities or nutritionally essential resources.