It has been proposed that the invariant kinematics observed during goal-directed movements result from reducing the consequences of signal-dependent noise (SDN) on motor output. The purpose of this study was to investigate the presence of SDN during isometric force production and determine how central and peripheral components contribute to this feature of motor control. Peripheral and central components were distinguished experimentally by comparing voluntary contractions to those elicited by electrical stimulation of the extensor pollicis longus muscle. To determine other factors of motor-unit physiology that may contribute to SDN, a model was constructed and its output compared with the empirical data. SDN was evident in voluntary isometric contractions as a linear scaling of force variability (SD) with respect to the mean force level. However, during electrically stimulated contractions to the same force levels, the variability remained constant over the same range of mean forces. When the subjects were asked to combine voluntary with stimulation-induced contractions, the linear scaling relationship between the SD and mean force returned. The modeling results highlight that much of the basic physiological organization of the motor-unit pool, such as range of twitch amplitudes and range of recruitment thresholds, biases force output to exhibit linearly scaled SDN. This is in contrast to the square root scaling of variability with mean force present in any individual motor-unit of the pool. Orderly recruitment by twitch amplitude was a necessary condition for producing linearly scaled SDN. Surprisingly, the scaling of SDN was independent of the variability of motoneuron firing and therefore by inference, independent of presynaptic noise in the motor command. We conclude that the linear scaling of SDN during voluntary isometric contractions is a natural by-product of the organization of the motor-unit pool that does not depend on signal-dependent noise in the motor command. Synaptic noise in the motor command and common drive, which give rise to the variability and synchronization of motoneuron spiking, determine the magnitude of the force variability at a given level of mean force output.