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Bahrain location in the Arabian Gulf contributed to the diversity of its indigenous population descended from Christian Arabs, Persians (Zoroastrians), Jews, and Aramaic-speaking agriculturalists. The aim of this study was to examine population substructure within Bahrain using the 27 Y-STRs (short tandem repeats) in the Yfiler Plus kit and to characterize the haplotypes of 562 unrelated Bahraini nationals, sub-divided into the four geographical regions - North, Capital, South and Muharraq. Yfiler Plus provided a significant improvement over the earlier 17-locus Yfiler kit in discrimination capacity, increasing it from 77% to 87.5%, but this value differed widely between regions from 98.4% in Muharraq to 75.2% in the Northern region, an unusually low value possibly as a consequence of the very rapid expansion in population size in the last 80 years. Clusters of closely related male lineages were seen, with only 79.4% of donors displaying unique haplotypes and 59% of instances of shared haplotypes occurring within, rather than between, regions. Haplogroup prediction indicated diverse origins of the population with a predominance of haplogroups J2 and J1, both typical of the Arabian Peninsula, but also haplogroups such as B2 and E1b1a originating in Africa and H, L and R2 indicative of migration from the east. Haplogroup frequencies differed significantly between regions with J2 significantly more common in the Northern region compared with the Southern possibly as a result of differential settlement with Baharna (descended from populations in which J2 predominates) and Arabs (both indigenous and migrant Huwala who are expected to have a higher frequency of J1). Our study illustrated the importance of encompassing geographical and social variation when constructing population databases and the need for highly discriminating multiplexes where rapid expansions have occurred within tightly bounded populations.