Homeostatic regulation ensures stable neural circuit output under changing conditions. In Drosophila larvae, either pre-synaptic weakening due to perturbation of transmitter release or postsynaptic weakening due to perturbation of glutamate receptors at synapses between motor neuron (MN) and muscle has little impact on locomotion, suggesting a non-synaptic compensatory mechanism. In vivo imaging shows that five different forms of synaptic weakening all increase the duration of activity bouts in MNs. A dual mechanism underlies this effect:  a cell-autonomous adjustment of MN excitability and a circuit adjustment of inhibitory central drive. The effect is input-selective, affecting only tonic MNs, which receive input from homeostatically adjusting premotor neurons and not phasic MNs, which do not. Thus, decrease in synaptic transmission per action potential is compensated by an increase in action potential number, but only to maintain tonic drive, while holding constant the phasic drive that organizes locomotory wave patterns