How long does it take for a neuron to return to it's resting state, due to absence of further stimulus?
Neurons (either the neuron as a whole, or segments such as a length of dendrite) can be modeled as an RC circuit. This is because the membrane acts as both a resistor and capacitor.
RC circuits have a time constant tau, equal to R * C. This time constant describes how long it takes to passively discharge the membrane capacitor.
In the context of neurons, this is referred to as the "membrane time constant" and like other exponential decay constants it refers to the amount of time that passes before the voltage has gone ~63.2% of the way towards rest.
In exponential decay, equilibrium is never truly reached, but after ~2-3 time constants it is likely decayed to within measurement precision given other sources of noise.
To answer your question "how long" the only answer is "it depends" - neurons with different functions have very different time constants. Time constants also aren't perfectly static, because the membrane resistance is not constant due to channels gated by voltage or signalling molecules. Typical values are from milliseconds to tens of milliseconds.