Plants are master chemists and collectively are able to produce hundreds of thousands of different organic compounds. The genes underlying the biosynthesis of many specialized metabolites are organized in biosynthetic gene clusters (BGCs), which is hypothesized to ensure their faithful coinheritance and to facilitate their coordinated expression. In rice (Oryza sativa), momilactones are diterpenoids that act in plant defence and various organismic interactions. Many of the genes essential for momilactone biosynthesis are grouped in a BGC. We applied comparative genomics of diploid and allotetraploid Oryza species to reconstruct the species-specific architecture, evolutionary trajectory, and sub-functionalisation of the momilactone biosynthetic gene cluster (MBGC) in the Oryza genus. Our data show that the evolution of the MBGC is marked by lineage-specific rearrangements and gene copy number variation, as well as by occasional cluster loss. We identified a distinct cluster architecture in Oryza coarctata, which represents the first instance of an alternative architecture of the MBGC in Oryza and strengthens the idea of a common origin of the cluster in Oryza and the distantly related genus Echinochloa. Our research illustrates the evolutionary and functional dynamics of a biosynthetic gene cluster within a plant genus.