Chromatin remodelers can either organize or disrupt nucleosomal arrays, yet the mechanisms specifying these opposing actions are not clear. Here, we show that the outcome of nucleosome sliding by Chd1 changes dramatically depending on how the chromatin remodeler is targeted to nucleosomes. Using a Chd1-streptavidin fusion remodeler, we found that targeting via biotinylated DNA resulted in directional sliding towards the recruitment site, whereas targeting via biotinylated histones produced a distribution of nucleosome positions. Remarkably, the fusion remodeler shifted nucleosomes with biotinylated histones up to 50 bp off the ends of DNA and was capable of reducing negative supercoiling of plasmids containing biotinylated chromatin, similar to remodelling characteristics observed for SWI/SNF-type remodelers. These data suggest that forming a stable attachment to nucleosomes via histones, and thus lacking sensitivity to extranucleosomal DNA, seems to be sufficient for allowing a chromatin remodeler to possess SWI/SNF-like disruptive properties.