Countershading is a ubiquitous patterning of animals whereby the side that typically faces the highest illumination is darker. When tuned to specific lighting conditions and body orientation with respect to the light field, countershading minimizes the gradient of light the body reflects by counterbalancing shadowing due to illumination, and has therefore classically been thought of as an adaptation for visual camouflage. However, whether and how crypsis degrades when body orientation with respect to the light field is non-optimal has never been studied. We tested the behavioural limits on body orientation for countershading to deliver effective visual camouflage. We asked human participants to detect a countershaded target in a simulated three-dimensional environment. The target was optimally coloured for crypsis in a reference orientation and was displayed at different orientations. Search performance dramatically improved for deviations beyond 15 degrees. Detection time was significantly shorter and accuracy significantly higher than when the target orientation matched the countershading pattern. This work demonstrates the importance of maintaining body orientation appropriate for the displayed camouflage pattern, suggesting a possible selective pressure for animals to orient themselves appropriately to enhance crypsis.