Timing and its variability are crucial for behavior. Consequently, neural circuits that take part in the control of timing and in the measurement of temporal intervals have been the subject of much research. Here, we provide an analytical and computational account of the temporal variability in what is perhaps the most basic model of a timing circuit, the synfire chain. First, we study the statistical structure of trial-to-trial timing variability in a reduced but analytically tractable model: a chain of single integrate-and-fire neurons. We show that this circuit’s variability is well-described by a generative model consisting of local, global, and jitter components. We relate each of these components to distinct neural mechanisms in the model. Next, we establish in simulations that these results carry over to a noisy homogeneous synfire chain. Finally, motivated by the fact that a synfire chain is thought to underlie the circuit that takes part in the control and timing of zebra finch song, we present simulations of a biologically realistic synfire chain model of the zebra finch timekeeping circuit. We find the structure of trial-to-trial timing variability to be consistent with our previous findings, and to agree with experimental observations of the song’s temporal variability. Our study therefore provides a possible neuronal account of behavioral variability in zebra finches. ### Competing Interest Statement The authors have declared no competing interest.