It is well known that eukaryotic cells can sense oxygen (O 2 ) and adapt their metabolism accordingly. It is less known that they can also move towards regions of higher oxygen level (aerotaxis). Using a self-generated hypoxic assay, we show that the social amoeba Dictyostelium discoideum displays a spectacular aerotactic behavior. When a cell colony is covered by a coverglass, cells quickly consume the available O 2 and the ones close to the periphery move directionally outward forming a dense ring keeping a constant speed and density. To confirm that O 2 is the main molecular player in this seemingly collective process, we combined two technological developments, porphyrin based O 2 sensing films and microfluidic O 2 gradient generators. We showed that Dictyostelium cells exhibit aerotactic and aerokinetic (increased speed at low O 2 ) response in an extremely low range of O 2 concentration (0-1.5%) indicative of a very efficient detection mechanism. The various cell behaviors under self-generated or imposed O 2 gradients were modeled with a very satisfactory quantitative agreement using an in silico cellular Potts model built on experimental observations. This computational model was complemented with a parsimonious ‘Go or Grow’ partial differential equation (PDE) model. In both models, we found that the collective migration of a dense ring can be explained by the interplay between cell division and the modulation of aerotaxis, without the need for cell-cell communication. Explicit wave solutions of the PDE model also informed about the relative contributions of division and directed motion on the collective speed.