Until recently, much of the microbial world was hidden from view. A global research effort has changed this, unveiling and quantifying microbial diversity across enormous range of critically-important contexts, from the human microbiome, to plant-soil interactions, to marine life. Yet what has remained largely hidden is the interplay of ecological and evolutionary processes that led to the diversity we observe in the present day. We introduce a theoretical framework to quantify the effect of ecological innovations in microbial evolutionary history, using a new, coarse-grained approach that is robust to the incompleteness and ambiguities in microbial community data. Applying this methodology, we identify a balance of gradual, ongoing diversification and rapid bursts across a vast range of microbial habitats. Moreover, we find universal quantitative similarities in the tempo of diversification, independent of habitat type.