Population declines resulting from anthropogenic activities are of major consequence for the long-term survival of species because the resulting loss of genetic diversity can lead to extinction via the effects of inbreeding depression, fixation of deleterious mutations, and loss of adaptive potential. Otariid pinnipeds have been exploited commercially to near extinction with some species showing higher demographic resilience and recolonization potential than others. The New Zealand fur seal (NZFS) was heavily impacted by commercial sealing between the late 18th and early 19th centuries, but has recolonized its former range in southern Australia. The species has also recolonized its former range in New Zealand, yet little is known about the pattern of recolonization. Here, we first used 11 microsatellite markers (n = 383) to investigate the contemporary population structure and dispersal patterns in the NZFS (Arctocephalus forsteri). Secondly, we model postsealing recolonization with 1 additional mtDNA cytochrome b (n = 261) marker. Our data identified 3 genetic clusters: an Australian, a subantarctic, and a New Zealand one, with a weak and probably transient subdivision within the latter cluster. Demographic history scenarios supported a recolonization of the New Zealand coastline from remote west coast colonies, which is consistent with contemporary gene flow and with the species’ high resilience. The present data suggest the management of distinct genetic units in the North and South of New Zealand along a genetic gradient. Assignment of individuals to their colony of origin was limited (32%) with the present data indicating the current microsatellite markers are unlikely sufficient to assign fisheries bycatch of NZFSs to colonies.