ALT Chromatin plays a pivotal role in genome expression, maintenance, and replication. To better understand chromatin organization, we developed a novel proximity-tagging method which assigns unique DNA barcodes to molecules that associate in 3D space. Using this method – Proximity Copy Paste (PCP) – we mapped the connectivity of individual nucleosomes in Saccharomyces cerevisiae. We show that chromatin is predominantly organized into regularly spaced nucleosome arrays whose properties differ according to transcriptional activity. Additionally, by mapping long-range, multi-way interactions we provide evidence that metaphase chromosomes are compacted by arrayed cohesin hubs. Using single-molecule nuclease footprinting data we define distinct chromatin states within a mixed population to show that noncanonical nucleosomes are a stable feature of chromatin. PCP is a versatile method allowing the connectivity of individual molecules to be mapped at high-resolution.