Skin microbiomes provide vital functions, yet knowledge about their species assemblages is limited - especially for non-model organisms. In this study, we conducted in situ manipulations and repeated sampling on wild-caught individuals of Rutilus rutilus. Treatments included translocation between fresh and brackish water habitats to investigate the role of environment; community rebooting by disinfection to infer host-microbe interactions; and housing in pairs to study the role of inter-host dispersal for the structure of microbiomes colonizing animals. Results revealed that fish skin microbiomes were biodiversity hotspots with highly dynamic composition that were distinct from bacterioplankton communities. External environmental conditions and individual-specific factors jointly determined the colonization-extinction dynamics, whereas inter-host dispersal had negligible effects. The dynamics of the microbiome composition was seemingly non-affected by reboot treatment, pointing to high resilience to disturbance in these microbial communities. Together, the manipulations demonstrate that host individual characteristics and environment interactively shapes the skin microbiome of fish. The results emphasize the role of inter-individual variability for the unexplained variation found in many host-microbiome systems, although the mechanistic underpinnings remain to be identified.