Many key bacterial pathogens are frequently carried asymptomatically, and the emergence and spread of these opportunistic pathogens can be driven, or mitigated, via demographic changes within the host population. These inter-host transmission dynamics combine with basic evolutionary parameters such as rates of mutation and recombination, population size and selection, to shape the genetic diversity within bacterial populations. Whilst many studies have focused on how molecular processes underpin bacterial population structure, the impact of host migration and the connectivity of the local populations has received far less attention. A stochastic neutral model incorporating heightened local transmission has been previously shown to fit closely with genetic data for several bacterial species. However, this model did not incorporate transmission limiting population stratification, nor the possibility of migration of strains between subpopulations, which we address here by presenting an extended model. The model captures the observed population patterns for the common nosocomial pathogens Staphylococcus epidermidis and Enterococcus faecalis, while Staphylococcus aureus and Enterococcus faecium display deviations attributable to adaptation. It is demonstrated analytically and numerically that expected strain relatedness may either increase or decrease as a function of increasing migration rate between subpopulations, being a complex function of the rate at which microepidemics occur in the metapopulation. Moreover, it is shown that in a structured population markedly different rates of evolution may lead to indistinguishable patterns of relatedness among bacterial strains; caution is thus required when drawing evolution inference in these cases.