No published information is available on the foraging ecology and choice of feeding habitat of New Zealand’s rarest breeding bird: the New Zealand Fairy Tern (NZFT) Sternula nereis davisae. To address this gap, we conducted an assessment of the largest remaining breeding population at Mangawhai Harbour, Northland, New Zealand, during the chick-rearing period of the 2010/2011 breeding season. We combined visual tracking of birds with prey surveys and stable isotope analyses, and we present the first quantitative assessment of NZFT foraging. We recorded 405 foraging dives that show NZFT foraging habitat includes the water edges, shallow channels, and pools on the tidal flats of mangrove-lined (Avicennia marina var. resinifera) parts of the estuary; tidal pools on mud- and sandflats in the mid-estuary and lower harbour; the shallow margins of the dredged main channel in the lower harbour; the oxbow lagoons on the sand spit; and coastal shallows. Our study identifies the mangrove-lined highly tidal and shallow mid-estuary and the lagoon on the sand spit as foraging hotspots for the Mangawhai breeding population of the NZFT. The prey survey employed a seine-net sampling method at identified NZFT foraging sites and yielded 4,367 prey-sized fish of 11 species, two of which had not previously been reported in Mangawhai Harbour, as well as numerous shrimps. The most abundant fish were gobies of the genus Favonigobius. Our stable isotope results highlight gobies as the most important prey for NZFT chick rearing, also indicating that flounder Rhombosolea sp. contribute to NZFT diet. We raise the possibility that shrimps may also constitute a substantial diet component for NZFT, potentially providing up to 21% of diet mass for adult birds. While our results provide a first basis to understanding the feeding ecology of NZFT during their breeding season in order to facilitate conservation planning, further research is required to address inter-annual variation and to identify key foraging grounds for this Critically Endangered bird at other breeding sites.