ABSTRACT We utilize theoretical models of Population III stellar + nebular spectra to investigate the prospects of observing and accurately identifying Population III galaxies with JWST using both deep imaging and spectroscopy. We investigate a series of different colour cuts, finding that a combination of NIRCam and MIRI photometry through the F444W−F560W, F560W−F770W colours offers the most robust identifier of potential z = 8 Pop III candidates. We calculate that NIRCam will have to reach ∼28.5–30.0 AB mag depths (1–20 h), and MIRI F560W must reach ∼27.5–29.0 AB mag depths (10–100 h) to achieve 5σ continuum detections of M* = 106 M⊙ Pop III galaxies at z = 8. We also discuss the prospects of identifying Pop III candidates through slitless and NIRSpec spectroscopic surveys that target Lyα, Hβ, and/or He ii λ1640. We find small differences in the Hβ rest-frame equivalent width (EW) between Pop III and non-Pop III galaxies, rendering this diagnostic likely impractical. Instead, we find that the detection of high EW He ii λ1640 emission will serve as the definitive Pop III identifier, requiring (ultra-)deep integrations (5–150 h) with NIRSpec/G140M for M* = 106 M⊙ Pop III galaxies at z = 8. However, MIRI F770W detections of Pop III galaxies will require substantial gravitational lensing (μ = 10) and/or fortuitous imaging of exceptionally massive (M* = 107 M⊙) Pop III galaxies. Thus, NIRCam medium-band imaging surveys that can search for high EW He ii λ1640 emitters in photometry may perhaps be a viable alternative for finding Pop III candidates.