The specific patterns and functional properties of electrical synapses of a nervous system are defined by the neuron-specific complement of electrical synapse constituents. We systematically examined the molecular composition of the electrical connectome of the nematode C. elegans through a genome- and nervous-system-wide analysis of the expression patterns of the invertebrate electrical synapse constituents, the innexins. We observe highly complex combinatorial expression patterns throughout the nervous system and found that these patterns change in a strikingly neuron-type-specific manner throughout the nervous system when animals enter an insulin-controlled diapause arrest stage under harsh environmental conditions, the dauer stage. By analyzing several individual synapses, we demonstrate that dauer-specific electrical synapse remodeling is responsible for specific aspects of the altered locomotory and chemosensory behavior of dauers. We describe an intersectional gene regulatory mechanism involving terminal selector and FoxO transcription factors mediating dynamic innexin expression plasticity in a neuron-type- and environment-specific manner. Display omitted •Mapped complex, neuron-type-specific combinatorial patterns of innexin expression•The neuron-specific innexin expression code shows remarkable plasticity under stress•Altered innexin expression leads to circuit modification and behavioral plasticity•A FoxO-dependent combinatorial mechanism controls spatiotemporal innexin plasticity Mapping the electrical connectome of C. elegans reveals the combinatorial patterns of synaptic protein expression that dictate behaviors associated with the physiological state of the animal.