I detail four major open problems in microbial population genetics with direct implications to the study of molecular evolution: the lack of neutral polymorphism, the modeling of promiscuous genetic exchanges, the genetics of ill-defined populations, and the difficulty of untangling selection and demography in the light of these issues. Together with the historical focus on the study of single nucleotide polymorphism and widespread non-random sampling, these problems limit our understanding of the genetic variation in bacterial populations and their adaptive effects. I argue that we need novel theoretical approaches accounting for pervasive selection and strong genetic linkage to better understand microbial evolution.