Protected areas are often proposed as tools for conserving endangered populations of marine megafauna. Our study area includes a voluntary no-entry reserve embedded within wider critical habitat for Threatened ‘northern resident’ killer whales under Canada’s Species at Risk Act. Our study quantified the reserve’s importance to whales by assessing habitat preference in a behavioural context, and population-level implications of that preference given threats from human activities, such as oil spills resulting from shipping traffic. We recorded summertime activities of whales from 1995 to 2002. Whales were observed on 397 of 530 (74.9%) days. Whales showed strong preference for the reserve over adjacent waters, and used it preferentially for feeding and beach-rubbing. While the area comprises ∼0.001% of the whales’ range, an overall average of 6.5% of the population was present each day. Frequently, >50% of this small population was aggregated in the restricted and heavily trafficked waterway of Johnstone Strait. Using the Potential Biological Removal equation, we calculated potential annual mortality limits (ML) of 2.2 animals. Mean group size in the area exceeded ML on 55.8% of days overall, and 98.8% of days when conditioning on whale presence. The whales’ high reliance on a trivial fraction of their range means that opportunities are routine for one stochastic, catastrophic event to cause population decline. On 20 August 2007, a barge loaded with ∼10,000 L of diesel sank in the area, exposing 25% of the population. This underscores the importance of identifying critical habitat for threatened populations, and ensuring meaningful protection.