Pacific herring Clupea pallasii and Atlantic herring C. harengus are sister species of Pliocene origin that now both occur in northeastern Europe. Atlantic herring is represented by a huge oceanic population and several small coastal populations in Norway, whereas Pacific herring prevails in the Eastern Barents Sea and White Sea. Two populations in Northern Norway, one in the marine Balsfjord and the other, a putatively unique landlocked Clupea population in the neighboring meromictic Lake Rossfjordvatn, are phenotypically similar to C. pallasii. The Balsfjord herring is predominantly of C. pallasii genetic ancestry, but with 25% of C. harengus genes. Here we address hypotheses of the genetic composition and history of the Rossfjordvatn herring using mitochondrial cytochrome b sequencing and genotyping of microsatellite and allozyme marker genes. The Rossfjordvatn herring is a close relative, but not identical to the Balsfjord herring, with an estimated 30% of Atlantic herring nuclear genes, and 50% of Atlantic mtDNA. Mitochondrial diversity was less in Rossfjordvatn than in Balsfjord, with no shared Atlantic haplotypes between the samples. Assuming a recent common ancestry of these two populations, we hypothesize that the differences are due to drift and possibly also to independent hybridization with the Atlantic herring. With the new data, we reassess and corroborate the hypothesis of Laakkonen et al. (2015) that multiple admixed herring populations exist in Norway and discuss the role that extreme conditions in marine lakes may have in supporting hybrid populations.