There are several competing hypotheses on tooth origins, with discussions eventually settling in favour of an 'outside-in' scenario, in which internal odontodes (teeth) derived from external odontodes (skin denticles) in jawless vertebrates. The evolution of oral teeth from skin denticles can be intuitively understood from their location at the mouth entrance. However, the basal condition for jawed vertebrates is arguably to possess teeth distributed throughout the oropharynx (i.e. oral and pharyngeal teeth). As skin denticle development requires the presence of ectoderm-derived epithelium and of mesenchyme, it remains to be answered how odontode-forming skin epithelium, or its competence, were 'transferred' deep into the endoderm-covered oropharynx. The 'modified outside-in' hypothesis for tooth origins proposed that this transfer was accomplished through displacement of odontogenic epithelium, that is ectoderm, not only through the mouth, but also via any opening (e.g. gill slits) that connects the ectoderm to the epithelial lining of the pharynx (endoderm). This review explores from an evolutionary and from a developmental perspective whether ectoderm plays a role in (pharyngeal) tooth and denticle formation. Historic and recent studies on tooth development show that the odontogenic epithelium (enamel organ) of oral or pharyngeal teeth can be of ectodermal, endodermal, or of mixed ecto-endodermal origin. Comprehensive data are, however, only available for a few taxa. Interestingly, in these taxa, the enamel organ always develops from the basal layer of a stratified epithelium that is at least bilayered. In zebrafish, a miniaturised teleost that only retains pharyngeal teeth, an epithelial surface layer with ectoderm-like characters is required to initiate the formation of an enamel organ from the basal, endodermal epithelium. In urodele amphibians, the bilayered epithelium is endodermal, but the surface layer acquires ectodermal characters, here termed 'epidermalised endoderm'. Furthermore, ectoderm-endoderm contacts at pouch-cleft boundaries (i.e. the prospective gill slits) are important for pharyngeal tooth initiation, even if the influx of ectoderm via these routes is limited. A balance between sonic hedgehog and retinoic acid signalling could operate to assign tooth-initiating competence to the endoderm at the level of any particular pouch. In summary, three characters are identified as being required for pharyngeal tooth formation: (i) pouch-cleft contact, (ii) a stratified epithelium, of which (iii) the apical layer adopts ectodermal features. These characters delimit the area in which teeth can form, yet cannot alone explain the distribution of teeth over the different pharyngeal arches. The review concludes with a hypothetical evolutionary scenario regarding the persisting influence of ectoderm on pharyngeal tooth formation. Studies on basal osteichthyans with less-specialised types of early embryonic development will provide a crucial test for the potential role of ectoderm in pharyngeal tooth formation and for the 'modified outside-in' hypothesis of tooth origins.