Strong selection has resulted in substantial morphological and behavioural diversity across modern dog breeds, which makes dogs interesting model animals to study the underlying genetic architecture of these traits. However, results from between‐breed analyses may confound selection signatures for behaviour and morphological features that were co‐selected during breed development. In this study, we assess population genetic differences in a unique resource of dogs of the same breed but with systematic behavioural selection in only one population. We exploit these different breeding backgrounds to identify signatures of recent selection. Selection signatures within populations were found on chromosomes 4 and 19, with the strongest signals in behaviour‐related genes. Regions showing strong signals of divergent selection were located on chromosomes 1, 24 and 32, and include candidate genes for both physical features and behaviour. Some of the selection signatures appear to be driven by loci associated with coat colour (Chr 24; ASIP ) and length (Chr 32; FGF5 ), while others showed evidence of association with behaviour. Our findings suggest that signatures of selection within dog breeds have been driven by selection for morphology and behaviour. Furthermore, we demonstrate that combining selection scans with association analyses is effective for dissecting the traits under selection.