Understanding the divergence of behavioural signals in isolated populations is critical to knowing how certain barriers to gene flow can develop. For many bird species, songs are essential for conspecific recognition and mate choice. Measuring the rate of song divergence in natural populations is difficult, but translocations of endangered birds to isolated islands for conservation purposes can yield insights, as the age and source of founder populations are completely known. We found significant and rapid evolution in the structure and diversity of bird song in North Island saddlebacks, Philesturnus rufusater, in New Zealand, with two distinct lineages evolving in < 50 years. The strong environmental filters of serial translocations resulted in cultural bottlenecks that generated drift and reduced song variability within islands. This rapid divergence coupled with loss of song diversity has important implications for the behavioural evolution of this species, demonstrating previously unrecognised biological consequences of conservation management.