Multicellular eukaryotic organisms contain identical genetic information within each cell, stored within the nucleus as chromatin fibers. The regulation of gene expression allows cell-type-specific temporal and spatial gene activation or repression despite the identical DNA sequence that determines differentiation and cell identity. Chromatin 'writer' enzymes can alter chromatin by installing post-translational modifications (PTMs) on histone proteins, which are then recognized by 'reader' proteins. PTMs are epigenetic marks that regulate a dynamic yet balanced gene expression. Polycomb group (PcG) proteins form a regulatory system of 'readers' and 'writers', essential for transcriptional repression during development and differentiation. Polycomb repressive complexes 1 (PRC1), a key member of the PcG family, function as the primary E3 ligase 'writers' of ubiquitination on histone H2A at lysine 119 (H2AK119ub). The H2AK119ub modification recruits Polycomb repressive complexes 2 (PRC2) to install H3K27me1-3 and form repressive chromatin domains. Thus, variant PRC1 (vPRC1) is the primary catalyst of PcG-initialized gene repression, with its activity dependent on its multisubunit composition, among others, the Polycomb group of ring finger (PCGF) subunit. vPRC1 complexes dynamically engage chromatin, but how these transient interactions are coupled to ubiquitin writing is unknown. Here, I present a single-molecule fluorescence approach to directly observe ubiquitination dynamics by vPRC1 in real-time on defined chromatin. Initially, I dissected the recruitment dynamics of PRC1 complexes on immobilized synthetic chromatin. Subsequently, I introduced vPRC1 with a preloaded E2~Ub to initiate H2AK119 ubiquitination. The observed binding and enzymatic kinetics were used to construct a mechanistic model of real-time chromatin 'reading' and 'writing'. vPRC1 transiently recruited chromatin fibers with non-specific and specific binding modes characterized by short and long residence times. The presence of E2 increased the specific residence time and the association rate, while a pre-installed H2AK119ub rescued the dissociation and association times observed on wild-type chromatin. vPRC1 complexes dynamically searched chromatin until they bound nucleosomes in a catalytically competent state, followed by E2~Ub recruitment and ubiquitin transfer. The ubiquitination rate increased over time on wild-type H2A chromatin fibers, while the ubiquitination efficiency on H2AK119R/K120R was minimal. vPRC1 showed a small processivity with up to two ubiquitin being transferred per single binding event. The reactive binding and catalytic times of isolated events were independent of vPRC1 subunit composition, while PCGF1-containing enzymes showed faster global ubiquitination due to more frequent catalytically competent states. The efficiency of E2~Ub recruitment and the formation of the catalytically active state determined the global activity differences between PRC1 subtypes containing either PCGF1 or PCGF4. The findings demonstrate that the key factor influencing vPRC1 ubiquitination activity is the dynamic assembly of a ternary complex between chromatin, vPRC1 and E2. The methodology may be expanded to study the enzymatic kinetics of other E3 ligase enzymes and deubiquitinases on chromatin or other substrates. In particular, single-molecule enzymology can be applied to characterize drugs' effects on the binding and enzymatic kinetics of E3 ligas