The assessment of fine-scale population structure is critical for the conservation and management of the European dark honey bee (Apis mellifera mellifera). Wing geometric morphometrics and molecular marker panels remain the principal tools for identifying honeybee origins and delineating subspecies. However, previous studies have primarily focused on quantifying admixture levels in Western honeybees (Apis mellifera), while assessments of inbreeding and genetic contribution and its potential consequences for population integrity have received far less attention. To address this gap, we complemented admixture analyses with estimates of individual genetic contributions and inbreeding levels of Apis mellifera and integrated these metrics into a high-resolution network visualization. We analyzed 380 honey bees (283 workers and 97 drone-pools) from 14 European breeding populations, including recently established Bosland population of Apis mellifera mellifera, genotyped at 70,814 genome-wide SNPs. Runs of homozygosity analysis revealed considerable variation within the Bosland population, where a subset of drone-pools and workers exhibited low genomic inbreeding levels, reflecting high admixture, whereas C-lineage (Apis mellifera carnica and Apis mellifera ligustica) workers also exhibited low inbreeding. In contrast, Apis mellifera mellifera from three French islands and Apis mellifera mellifera drone pools showed on average the highest inbreeding values. High-resolution network visualization effectively resolved population structure, clearly distinguishing M- from C-lineage, and captured fine-scale genetic relatedness, enabling the identification of relationships among sister workers and sister queens, as well as between queens and their offspring. Overall, our results provide a robust framework for genomics-informed monitoring and conservation of A. m. mellifera and demonstrate the utility of medium-density SNP data for resolving both fine-scale population structure and genomic inbreeding.