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Chromosomal inversions, by suppressing recombination, can profoundly shape genome evolution and drive adaptation. In the common quail (Coturnix coturnix), a highly mobile bird with a vast Palearctic breeding range, we previously identified a massive inversion on chromosome 1 associated with distinct phenotypes and restricted geographic distribution. Here, using a new de novo genome assembly, we characterise this inversion and uncover additional, ancient structural variation on chromosome 2 that segregates across the species' range: either two putatively linked inversions or a single, large inversion that appears as two due to scaffolding limitations. Together, the inversions encompass a remarkable 15.6% of the quail genome (153.6 Mbp), creating highly divergent haplotypes that diverged over a million years ago. While the chromosome 1 inversion is linked to phenotypic differences, including morphology and migratory behaviour, the chromosome 2 inversion(s) show no such association. Notably, all inversion regions exhibit reduced effective population size and a relaxation of purifying selection, evidenced by elevated nonsynonymous-to-synonymous substitution ratios (N/S). This suggests that inversions, particularly the geographically restricted one on chromosome 1, may act as engines of diversification, accelerating the accumulation of functional variation and potentially contributing to local adaptation, especially within isolated island populations. Our findings demonstrate how large-scale chromosomal rearrangements can compartmentalise a genome, fostering distinct evolutionary trajectories within a single, highly mobile species.