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Adult human facial skin microbiomes are remarkably similar at the species level, dominated by Cutibacterium acnes and Staphylococcus epidermidis, yet each person harbors a unique community of strains. Understanding how person-specific communities assemble is critical for designing microbiome-based therapies. Here, using 4,055 isolate genomes and 356 metagenomes, we reconstruct on-person evolutionary history to reveal on- and between-person strain dynamics. We find that multiple cells are typically involved in transmission, indicating ample opportunity for migration. Despite this accessibility, family members share only some of their strains. S. epidermidis communities are dynamic, with each strain persisting for an average of only 2 years. C. acnes strains are more stable and have a higher colonization rate during the transition to an adult facial skin microbiome, suggesting this window could facilitate engraftment of therapeutic strains. These previously undetectable dynamics may influence the design of microbiome therapeutics and motivate the study of their effects on hosts.