Collective migration occurs throughout the animal kingdom, and demands both the interpretation of navigational cues and the perception of other individuals within the group. Navigational cues orient individuals towards a destination, while it has been demonstrated that communication between individuals enhances navigation through a reduction in orientation error. We develop a mathematical model of collective navigation that synthesizes navigational cues and perception of other individuals. Crucially, this approach incorporates uncertainty inherent to cue interpretation and perception in the decision making process, which can arise due to noisy environments. We demonstrate that collective navigation is more efficient than individual navigation, provided a threshold number of other individuals are perceptible. This benefit is even more pronounced in low navigation information environments. In navigation ‘blindspots’, where no information is available, navigation is enhanced through a relay that connects individuals in information-poor regions to individuals in information-rich regions. As an expository case study, we apply our framework to minke whale migration in the northeast Atlantic Ocean, and quantify the decrease in navigation ability due to anthropogenic noise pollution.