Any biological process involving the genome – be it transcription, replication or repair – requires the remodelling of histone-DNA interactions. This remodelling is achieved by ATP-dependent DNA translocase enzymes. We set out to determine the mechanism by which one prominent remodeller – the CHD4 – can move histones relative to DNA. We have used single-molecule FRET measurements to demonstrate that the binding energy for CHD4-nucleosome complex formation – even in the absence of nucleotide –triggers significant conformational changes in DNA at the entry side, effectively priming the system for remodelling. During remodelling, flanking DNA enters the nucleosome in a continuous, gradual manner but exits in concerted 4–6 base-pair steps. This decoupling of entry- and exit-side translocation suggests that ATP-driven movement of entry-side DNA builds up strain inside the nucleosome that is subsequently released at the exit side by DNA expulsion. We propose a mechanism for nucleosome sliding based on these and published data.