Behaviours are often correlated within broader syndromes, creating the potential for evolution in one behaviour to drive evolutionary changes in other behaviours. Despite demonstrations that behavioural syndromes are common, this potential for evolutionary effects has not been demonstrated. Here we show that populations of field crickets ( Gryllus integer ) exhibit a genetically conserved behavioural syndrome structure, despite differences in average behaviours. We found that the distribution of genetic variation and genetic covariance among behavioural traits was consistent with genes and cellular mechanisms underpinning behavioural syndromes rather than correlated selection. Moreover, divergence among populations' average behaviours was constrained by the genetically conserved behavioural syndrome. Our results demonstrate that a conserved genetic architecture linking behaviours has shaped the evolutionary trajectories of populations in disparate environments—illustrating an important way for behavioural syndromes to result in shared evolutionary fates.