Mitochondrial DNA (mtDNA) sequences were analyzed from 106 bowhead whale (Balaena mysticetus) specimens dating 471 ± 44 14C b.p.–10,290 ± 150 14C b.p. to evaluate whether historical changes in distribution and connectivity were detectable in levels of diversity and population structuring in the Central Canadian Arctic. The species has maintained levels of mtDNA diversity over 10,000 yr comparable to other nonbottlenecked large whale species. When compared to data from the Holocene East Greenland/Spitsbergen and contemporary Bering-Chuckchi-Beaufort populations, differentiation was low (FST≤ 0.005, ΦST≤ 0.003) and no temporal or geographical genetic structuring was evident. A combination of analyses suggests that the population has expanded over the past 30,000 14C yr. This genetic signature of expansion could result from population growth, admixture of multiple gene pools, or a combination of both scenarios. Despite known climatic change that altered bowhead distribution and led to isolation of populations, there is no detectable population structuring or change in genetic diversity during the Holocene. This may be due to long generation time, occasional population connectivity and a historically large global population. These characteristics warrant caution when interpreting contemporary bowhead whale DNA data, as it is unlikely that any population will be in mutation-drift equilibrium.