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Oil spilled in marine environments can settle to the seafloor through aggregation and sedimentation processes. This has been predicted to be especially relevant in the Arctic due to plankton blooms initiated by melting sea ice. These conditions exist in the Kivalliq region in Nunavut, Canada, where elevated shipping traffic has increased the risk of accidental spills. Experimental microcosms combining surface sediment and crude oil were incubated at 4 °C over 21 weeks to evaluate the biodegradation potential of seabed microbiomes. Sediments sampled near the communities of Arviat and Chesterfield Inlet were assessed for biodegradation capabilities by combining hydrocarbon geochemistry with 16S rRNA gene and metagenomic sequencing, revealing decreased microbial diversity but enrichment of oil-degrading taxa. Alkane and aromatic hydrocarbon losses corresponded to detection of genes and genomes that encode enzymes for aerobic biodegradation of these compounds, pointing to the utility of marine microbiome surveys for predicting the fate of oil released into Arctic marine environments. [Display omitted] • Marine oil spill risks are linked to shipping in Kivalliq, Nunavut. • Permanently cold sediment microbiomes degrade alkane and aromatic hydrocarbons. • Biodegradation genes point to natural attenuation potential in the baseline microbiome. • Crude oil exposure enriches some taxa but causes decrease in microbial diversity. [ABSTRACT FROM AUTHOR]