Coffea arabica, an allotetraploid hybrid of C. eugenioides and C. canephora, is the source of approximately 60% of coffee products worldwide. Cultivated accessions have undergone several population bottlenecks resulting in low genetic diversity. We present chromosome-level assemblies of a di-haploid C. arabica accession and modern representatives of its diploid progenitors, C. eugenioides and C. canephora. The three species exhibit largely conserved genome structures between diploid parents and descendant subgenomes, which show a mosaic pattern of dominance, similar to other polyploid crop species. Resequencing of 39 wild and cultivated accessions suggests a founding polyploidy event ∼610,000 years ago, followed by several subsequent bottlenecks, including a population split ∼30.5 kya and a period of migration between Arabica populations until ∼8.9 kya. Analysis of lines historically introgressed with C. canephora highlights loci that may contribute to their superior pathogen resistance and lay the groundwork for future genomics-based breeding of C. arabica.