Understanding genetic diversity and gene flow within and between mussel populations informs population fitness and contributes towards aquaculture sustainability. Shetland, in the north of Scotland, is responsible for >60% of UK blue mussel production. As such, we aimed to investigate the genetic diversity and population structure of mussels grown in this important location compared with populations elsewhere in the north of Scotland. DNA was isolated from samples taken from four populations, each containing 30 animals: two from northeast mainland Scotland (Cromarty Firth); one from northwest of Scotland (Western Isles); and two populations of locally adapted Shetland mussels. Single Nucleotide Polymorphisms (SNPs) analysis was performed using a medium density multi-species Mytilus array. To analyse subspecies hybridisation, we also included reference samples of Mytilus subspecies: M. galloprovincialis, M. edulis and M. trossulus. The initial analysis reveals that Cromarty populations appear to predominantly have M. edulis genetics. On the other hand, mussels from Shetland and the Western Isles display levels of introgression with M. galloprovincialis. Higher levels of genetic conservation were seen in the Western Isles compared with the relatively diverse genetics observed in both Shetland populations. Further analysis of each population using Nanopore sequencing was carried out to explore the levels of large structural variation (SV) and Presence/Absence Variations (PAV) in stress-response genes. Taken together, these data demonstrate that this SNP array provided a robust platform for consistent genotyping of individuals and may be used to further investigate appropriate growing environments for background genetics to enhance mussel health and productivity.