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Summary 1. Megaplanktivores such as filter-feeding sharks and baleen whales are at the apex of a short food chain (phytoplankton‐zooplankton‐vertebrate) and are sensitive indicators of sea-surface plankton availability. Even though they spend the majority of their time below the surface it is still not known how most of these species utilize vertical habitat and adapt to short-term changes in food availability. 2. A key factor likely to control vertical habitat selection by planktivorous sharks is the diel vertical migration (DVM) of zooplankton; however, no study has determined whether specific ocean-habitat type influences their behavioural strategy. Based on the first high-resolution dive data collected for a plankton-feeding fish species we show that DVM patterns of the basking shark Cetorhinus maximus reflect habitat type and zooplankton behaviour. 3. In deep, well-stratified waters sharks exhibited normal DVM (dusk ascent‐dawn descent) by tracking migrating sound-scattering layers characterized by Calanus and euphausiids. Sharks occupying shallow, inner-shelf areas near thermal fronts conducted reverse DVM (dusk descent‐dawn ascent) possibly due to zooplankton predator‐prey interactions that resulted in reverse DVM of Calanus . 4. These opposite DVM patterns resulted in the probability of daytime-surface sighting differing between these habitats by as much as two orders of magnitude. Ship-borne surveys undertaken at the same time as trackings reflected these behavioural differences. 5. The tendency of basking sharks to feed or rest for long periods at the surface has made them vulnerable to harpoon fisheries. Ship-borne and aerial surveys also use surface occurrence to assess distribution and abundance for conservation purposes. Our study indicates that without bias reduction for habitat-specific DVM patterns, current surveys could under- or overestimate shark abundance by at least 10-fold.