The Western honey bee, Apis mellifera (A. mellifera) Linnaeus, is one of the world’s most economically important pollinators. Conserving genetic resources in this species is therefore of significant value. Despite this, little attention has been paid to the potential erosion of locally adapted genetic variants by transhumance of particular subspecies favoured by beekeepers. In particular, introgression and hybridisation by repeated backcrossing can disrupt naturally-selected allele combinations and therefore erode local adaptation. Here we use whole genome sequencing (WGS) to assess levels of introgression in the native subspecies Apis mellifera mellifera (A. m. mellifera) across a wide geographical scale in Britain and Ireland. Samples were obtained from both colonies maintained by individual beekeepers from non-imported stock and those outside of protected populations or specific breeding programmes. These were examined alongside sub-species reference samples from established refuges. ADMIXTURE and ABBA BABA analysis revealed that 17 out of 70 colonies showed no significant introgression. The remaining 53 colonies showed some evidence of introgression. This study underpins previous findings that Ireland harbours a large reservoir of A. m. mellifera. The Island of Colonsay (Scotland) and parts of the South West of England also harbour ‘pure’ colonies. New areas of interest for conservation are identified in Jersey, mainland Scotland and the Isle of Man. Our results are discussed in the context of implications for future research and conservation strategies of this globally important insect in its native range.