Invasive species are proliferating globally and cause a range of impacts, necessitating risk assessment and prioritization prior to management action. Experimentally derived estimates of per capita effects (e.g. functional responses) have been advocated as predictors of field impacts of potential invaders. However, risk assessments based on estimates from single populations can be misleading if per capita effects vary greatly across space and time. Here, we present a large-scale, multi-population comparison of per capita effects of the American spinycheek crayfish, Faxonius (formerly Orconectes) limosus—a species with an extensive invasion history in eastern North America and Europe. Functional responses were measured on individuals from six geographically disparate populations of F. limosus in its native and invaded ranges on two continents. These revealed inter-population differences in both the maximum feeding rate and functional response type that could not be explained by the biogeographic origin of the population nor by time since the invasion. We propose that other differences in source communities (including the presence of competitors) impose selective pressures for phenotypic traits that result in dissimilar per capita effects. We also compared functional responses of the congeners F. limosus and F. virilis in the presence and absence of potential competitors to examine indirect competitive effects on feeding behaviour. The maximum feeding rate of F. limosus, but not F. virilis, was suppressed in the presence of heterospecific and conspecific competitors, demonstrating how the per capita effects of these species can differ across biotic contexts. In the competitor-presence experiments, individuals from the invasive population of F. limosus consistently had a higher maximum feeding rate than those of the native F. virilis, regardless of treatment. Our results caution against invasion risk assessments that use information from only one (or a few) populations or that do not consider the biotic context of target habitats. We conclude that comparative functional responses offer a rapid assessment tool for invader ecological impacts under context dependencies when multiple populations are analyzed.