Gut motility undergoes a switch from myogenic to neurogenic control in late embryonic development. Here, we report on the first electrical events underlying neurogenic motility in the developing mouse, using a transgenic line expressing the GCamp6f reporter in neural crest cell derivatives. We find that both nitrergic inhibitory and cholinergic excitatory neurons exhibit spontaneous calcium activity and that this activity requires L-type calcium channels and intracellular store-operated calcium channels (IP3R). This spontaneous electrical activity translates in terms of motility in periodic, high-frequency contraction complexes, which are inhibited by tetrodotoxin. We demonstrate that the ENS is mechanosensitive from the earliest stages on (E14.5) and that this behavior is tetrodotoxin and 2-APB resistant, but requires synaptic transmission. We extend our result on spontaneous L-type channel-dependent spontaneous activity and TTX-resistant mechanosensitivity to the adult colon. Our results shed light on the critical transition from myogenic to neurogenic motility in the developing gut.