The inherently nonlinear dynamics of two surfaces as they are driven past each other, a phenomenon known as dry friction, has yet to be fully understood on an atomistic level. New experiments on colloidal monolayers forced over laser-generated substrates now offer the opportunity to investigate friction with single-particle resolution. Here, we use analytical theory and computer simulations to study the effect of thermal fluctuations on the stick-slip mechanism characteristic for the frictional response of a stiff colloidal monolayer on a commensurate substrate. By performing a harmonic expansion of the energy and employing elementary statistical mechanics, we map the motion of the monolayer onto a simple differential equation. Analytical expressions derived from our approach predict a transition from nucleation dynamics, where the monolayer moves in a sequence of activated hops over energy barriers, to “thermal sliding”, in which the effective substrate barrier opposing the motion of the monolayer disappears due to thermal fluctuations, leading to continuous, uninterrupted sliding motion. Furthermore, we find that the average velocity of the monolayer for large driving forces obeys a simple scaling behavior that is consistent with the existence of a static friction. For small forces, however, nucleation provides a mode of motion that leads to a small but non-vanishing mobility of the monolayer. Data obtained from simulations confirm this picture and agree quantitatively with our analytical formulae. The theory developed here holds under general conditions for sufficiently strong inter-particle repulsions and it yields specific predictions that can be tested in experiments.