Genome annotation is critical to understand the function of disease variants, especially for clinical applications. To meet this need there are segmentations available from public consortia reflecting varying unsupervised approaches to functional annotation based on epigenetics data, but there remains a need for transparent, reproducible, and easily interpreted genomic maps of the functional biology of chromatin. We introduce a new methodological framework for defining a combinatorial epigenomic model of chromatin state on a web database, StateHub. In addition, we created an annotation tool for bioconductor, StatePaintR, which accesses these models and uses them to rapidly (on the order of seconds) produce chromatin state segmentations in standard genome browser formats. Annotations are fully documented with change history and versioning, authorship information, and original source files. StatePaintR calculates ranks for each state from next-gen sequencing peak statistics, facilitating variant prioritization, enrichment testing, and other types of quantitative analysis. StateHub hosts annotation tracks for major public consortia as a resource, and allows users to submit their own alternative models.