AbstractEnvironmental changes are prominent in Arctic ecosystems, where the distribution, abundance, life history, and health of marine organisms such as the bowhead whale (Balaena mysticetus) are tightly connected to sea ice and sea temperature. However, due to logistical and other challenges of data collection in the Arctic, appropriate assessments of past, present and future effects of climate change and human activities are lacking for many Arctic species. Environmental DNA (eDNA) is emerging as a noninvasive and cost‐effective way of obtaining genetic material from the environment and has the potential to complement traditional methods for biodiversity and genetic monitoring. In this study, we investigate whether eDNA isolated from seawater samples has the capacity to capture the genetic diversity of bowhead whales in Disko Bay, West Greenland, for the implementation of long‐term genetic monitoring programs of key Arctic marine species. A total of 41 eDNA “footprint” samples were obtained from the water surface after a whale had dived and an additional 54 eDNA samples were collected along transect lines. Samples were screened for bowhead DNA using a species‐specific qPCR primer and probe assay, and a subset of 30 samples were successfully Sanger‐sequenced to generate individual mitochondrial control region haplotypes. Moreover, by shotgun sequencing ten footprint samples on an Illumina NovaSeq platform we show that footprints generally contain less than 1% endogenous DNA, resulting in partial mitochondrial genomes in four samples out of ten samples. Our findings suggest that sampling in the footprint or wake of traveling animals is a promising method for capturing the genetic diversity of bowhead whales and other marine megafauna. With optimization of sampling and target DNA sequencing for higher endogenous DNA yield, seawater eDNA samples have a large potential for implementation in the long‐term population genetic monitoring of marine megafauna in the Arctic and elsewhere.