Population III (pop III) galaxies, made partly or exclusively of metal-free stars, are predicted to exist at high redshifts and may produce very strong Lyα emission. A substantial fraction of these Lyα photons are likely absorbed in the intergalactic medium at z > 6, but recent simulations suggest that significant Lyα emission may be detectable up to z≈ 8.5, i.e. well into the reionization epoch. Here, we argue that high-redshift pop III galaxies with strong Lyα emission can be identified in Hubble Space Telescope imaging data because of their unusual colours. We quantify this effect in some of the filters used in Y-band dropout searches for galaxies at z≈ 8 and find that pop III galaxies with high Lyα fluxes may exhibit much bluer J−H colours at z≈ 8–10 than any normal type of galaxy at these redshifts. This colour signature can arise even if pop III stars account for as little as ∼10−3 to 10−2 of the stellar mass in these galaxies. Some of the anomalously blue objects reported in current Y-band dropout samples do in fact meet the colour criteria for Lyα-emitting pop III galaxies.