Microbiomes are intricately intertwined with human health, geochemical cycles, and food production. While many microbiomes of interest are highly complex and experimentally intractable, cheese rind microbiomes have proven to be powerful model systems for the study of microbial interactions. To provide a more comprehensive view of the genomic potential and temporal dynamics of cheese rind communities, we combined longitudinal, multi-platform metagenomics of three ripening washed-rind cheeses with whole-genome sequencing of community isolates. Sequencing-based approaches revealed a highly reproducible microbial succession in each cheese and the coexistence of closely related Psychrobacter species and enabled the prediction of plasmid and phage diversity and their host associations. In combination with culture-based approaches, we established a genomic catalog and a paired 16-member in vitro washed-rind cheese system. The combination of multi-platform metagenomic time-series data and an in vitro model provides a rich resource for further investigation of cheese rind microbiomes both computationally and experimentally.