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Aim: The Eastern Afromontane Biodiversity Hotspot (EABH) offers an ideal location to investigate the evolutionary mechanisms producing a high level of endemic biodiversity. We tested the hypothesis that the cradle of Eastern Afromontane diversity is in the largest sub‐region of the EABH montane archipelago, that is the Ethiopian Highlands. Further, we expected that climate oscillations followed by elevational shifts in montane habitats facilitated the dispersal of small mammal populations across unsuitable arid lowlands. Location: Mountains and highlands of East Africa. Taxon: Shrews of the genus Crocidura (Eastern Afromontane phylogenetic clade). Methods: We collected comprehensive genetic data from 511 (mitochondrial gene for cytochrome b) and 147 (double digest Restriction‐Associated DNA sequencing) samples of Crocidura shrews across the EABH. We estimated phylogenetic relationships with Bayesian and Maximum Likelihood approaches. Population genetic analyses were performed in STRUCTURE to evaluate the internal structure of species outside Ethiopia. Ancestral area and dispersal routes were analysed by the BioGeoBears package. Results: Six major phylogenomic clades were delimited based on concatenated nuclear loci. The mitochondrial phylogeny roughly matches nuclear phylogenies, but with poorer resolution. Five of the six revealed clades are restricted to the Ethiopian Highlands, which is unambiguously the cradle of the diversity of this group of mammals (also confirmed by the biogeographic analysis). All non‐Ethiopian and a single Ethiopian species fall into the sixth clade with poorly resolved internal relationships. Detailed population genetic analysis of SNP data revealed a pronounced structure with multiple gene pools in this clade; however, this structure only partly corresponds with the current taxonomy. Main Conclusions: Eastern Afromontane Crocidura shrews originated in the Ethiopian Highlands. They radiated there, and through a single southward dispersal event across the Turkana depression, they colonised the rest of the EABH in response to diverse geomorphology and climatic changes during the Plio‐Pleistocene. [ABSTRACT FROM AUTHOR]