Timing is essential, but circadian clocks, which play a crucial role in timekeeping, are almost unaddressed in evolutionary ecology. A key property of circadian clocks is their free-running period length (τ), i.e. the time taken for a full cycle under constant conditions. Under laboratory conditions, concordance of τ with the ambient light–dark cycle confers major fitness benefits, but little is known about period length and its implications in natural populations. We therefore studied natural variation of circadian traits in a songbird, the great tit (Parus major), by recording locomotor activity of 98 hand-raised, wild-derived individuals. We found, unexpectedly, that the free-running period of this diurnal species was significantly shorter than 24 h in constant dim light. We furthermore demonstrate, to our knowledge for the first time in a wild vertebrate, ample genetic variation and high heritability (h2 = 0.86 ± 0.24), implying that period length is potentially malleable by micro-evolutionary change. The observed, short period length may be a consequence of sexual selection, as offspring from extra-pair matings had significantly shorter free-running periods than their half-siblings from within-pair matings. These findings position circadian clocks in the ‘real world’ and underscore the value of using chronobiological approaches in evolutionary ecology. Evolutionary ecologists study variation and its fitness consequences, but often have difficulties relating behavioural variation to physiological mechanisms. The findings presented here open the possibility that properties of internal, circadian clocks affect performance in traits that are relevant to fitness and sexual selection.