Advances in sequencing technologies mean that insights into crop diversification aiding future breeding can now be explored in crops beyond major staples. For the first time, we use a genome assembly of finger millet, an allotetraploid orphan crop, to analyze DArTseq single nucleotide polymorphisms (SNPs) at the sub-genome level. A set of 8,778 SNPs and 13 agronomic traits characterizing a broad panel of 423 landrace accessions from Africa and Asia suggested the crop has undergone complex, context-specific diversification consistent with a long domestication history. Both Principal Component Analysis and Discriminant Analysis of Principal Components of SNPs indicated four groups of accessions that coincided with the principal geographic areas of finger millet cultivation. East Africa, the considered origin of the crop, appeared the least genetically diverse. A Principal Component Analysis of phenotypic data also indicated clear geographic differentiation, but different relationships among geographic areas than genomic data. Neighbour-joining trees of sub-genomes A and B showed different features which further supported the crop’s complex evolutionary history. Our genome-wide association study indicated only a small number of significant marker-trait associations. We applied then clustering to marker effects from a ridge regression model for each trait which revealed two clusters of different trait complexity, with days to flowering and threshing percentage among simple traits, and finger length and grain yield among more complex traits. Our study provides comprehensive new knowledge on the distribution of genomic and phenotypic variation in finger millet, supporting future breeding intra- and inter-regionally across its major cultivation range.Core ideas8,778 SNPs and 13 agronomic traits characterized a panel of 423 finger millet landraces.4 clusters of accessions coincided with major geographic areas of finger millet cultivation.A comparison of phenotypic and genomic data indicated a complex diversification history.This was confirmed by the analysis of allotetraploid finger millet’s separate sub-genomes.Comprehensive new knowledge for intra- and inter-regional breeding is provided.