Activation of forebrain circuitry during sleep has been variably characterized as ‘pre- or replay’ and has been linked to memory consolidation. The evolutionary origins of this mechanism, however, are unknown. Sleep activation of the sensori-motor pathways of learned birdsong is a particularly useful model system because the muscles controlling the vocal organ are activated, revealing syringeal activity patterns for direct comparison with those of day-time vocal activity. Here we show that suboscine birds, which develop their species-typical songs innately without the elaborate forebrain-thalamic circuitry of the vocal learning taxa, also engage in replay during sleep. In two tyrannid species the characteristic syringeal activation patterns of song could also be identified during sleep. Similar to song-learning oscines, the burst structure was more variable during sleep than day-time song production. In kiskadees (Pitangus sulphuratus), a second vocalization, which is part of a multi-modal display, was also replayed during sleep along with one component of the visual display. These data show unambiguously that variable ‘replay’ of stereotyped motor programs is not restricted to programs confined within forebrain circuitry. The proposed effects on vocal motor program maintenance are therefore building on a pre-existing neural mechanism that predates the evolution of learned vocal motor behavior.