The exploration and exploitation of oil and gas resources in Canada’s Arctic carries with it certain risks that include the potential for oil spills and their effects on this fragile, yet extreme ecosystem. To develop an effective response strategy for an oil spill in an Arctic environment that would consist of a mixture of seawater and sea ice, a survey was conducted in the area of Cornwallis Island to develop baseline data on the natural microbial community structures and to determine whether these indigenous species possess the capacity to degrade petroleum hydrocarbons. Metagenomics and high throughput sequencing are relatively new approaches using modern genomics techniques to directly study communities of microorganisms in their natural environments, avoiding the need for traditional isolation and culturing. This provides more relevant ecological data, since the results directly relate to the population structure of the microorganisms that are present as well as the functional potential of the community, such as, for example, its inherent capacity to degrade petroleum hydrocarbons. Based on high-throughput sequencing of total community 16S rRNA gene amplicons and metagenomic sequencing, the indigenous bacterial populations in sea water were significantly different from those associated with the underside of the sea ice. Both sea water and sea ice were dominated by Bacteroidetes (Flavobacteria) but seawater was also abundant in Proteobacteria, primarily Alpha- and Gammaproteobacteria. The bottom of the sea ice demonstrated selective enrichment for Gammaproteobacteria, which contains numerous genera of obligate hydrocarbon degrading bacteria, such as Alkanivorax and Oleispira. There were both spatial and physicochemical influences on the microbial population structures, indicating that variations in the local environment can shape the structure of the microbial community, findings that are supported by other studies on polar microbial communities. These results demonstrate that seawater and sea ice in the Canadian Arctic possess natural microbial communities with the inherent ability to degrade petroleum hydrocarbons.