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Studies of innate colour preference and learning ability have focused on differences at the species level, rather than variation among populations of a single species. Initial strength and persistence of colour preferences are likely to affect colour choices of naïve flower visitors. We therefore study the influence of both the strength and persistence of innate colour preference (for blue) on an operant learning task (associating food reward with yellow flowers) in two populations of the bumblebee Bombus terrestris. We found that both strength and persistence of blue preference differed significantly between populations: B. terrestris dalmatinus had a weaker and less persistent blue preference than B. terrestris audax. These differences in preference also influenced learning performance. Considering only landing behaviours, one-trial learning occurred in the majority (73%) of bees, and was achieved sooner in B. terrestris dalmatinus because of its weaker blue preference. However, compared to landing behaviours the relative frequency of approach flights to rewarding and unrewarding flower types changed more slowly with task experience in both populations. When considering both approaches and landings, the rate of learning, following the first rewarded learning trial, was faster in B. terrestris audax than B. terrestris dalmatinus. However, the net effects of population differences in blue preference and learning dynamics result in similar final levels of task performance. Our results provide new evidence of behavioural differences among isolated populations within a single species, and raise intriguing questions about the ecological significance and adaptive nature of colour preference.