Despite technological advances in both tracking and sequencing technologies, finding the genetic mechanisms behind migratory traits remains a challenge. Recent studies have shown that migratory direction in European willow warblers (Phylloscopus trochilus) is mainly influenced by a repeat-rich region named MARB. Whether this genetic basis for orientation is unique to the willow warbler or instead shared by other closely related species is currently unknown. Therefore, here we investigate a close relative, the common chiffchaff (Phylloscopus collybita) by combining whole-genome resequencing data and geolocator tracks from two subspecies, P. c. collybita and P. c. abietinus. As in willow warblers, our geolocator data reveals that the two chiffchaff subspecies differ in orientation, with westward and eastward migratory directions from their breeding grounds in Sweden and south of the Baltics. Genome-wide divergence between the subspecies is low and consistent with a recent split within the last 100,000 years, as provided by demographic analyses. The divergence between subspecies is likely a result of shifts in allele frequencies across many loci although signals of differentiation are concentrated in the Z chromosome. Most differences, however, are found in the MARB region, raising the possibility that MARB contributes to orientation in chiffchaffs and may have evolved in parallel to willow warblers. Given the repeat-rich structure of this region, its characterization using short-read NGS sequencing remains challenging, and the diversity and nature of MARB haplotypes must be interpreted with caution.