Teff (Eragrostis tef) is a cornerstone of food security in the Horn of Africa, where it is prized for stress resilience, grain nutrition, and market value. Despite its overall importance to small-scale farmers and communities in Africa, teff suffers from low production compared to other cereals because of limited intensive selection and molecular breeding. Here we report a chromosome-scale genome assembly of allotetraploid teff (variety textquoteleftDabbitextquoteright) and patterns of subgenome dynamics. The teff genome contains two complete sets of homoeologous chromosomes, with most genes maintained as syntenic gene pairs. Through analyzing the history of transposable element activity, we estimate the teff polyploidy event occurred ~1.1 million years ago (mya) and the two subgenomes diverged ~5.0 mya. Despite this divergence, we detected no large-scale structural rearrangements, homoeologous exchanges, or bias gene loss, contrasting most other allopolyploid plant systems. The exceptional subgenome stability observed in teff may enable the ubiquitous and recurrent polyploidy within Chloridoideae, possibly contributing to the increased resilience and diversification of these grasses. The two teff subgenomes have partitioned their ancestral functions based on divergent expression patterns among homoeologous gene pairs across a diverse expression atlas. The most striking differences in homoeolog expression bias are observed during seed development and under abiotic stress, and thus may be related to agronomic traits. Together these genomic resources will be useful for accelerating breeding efforts of this underutilized grain crop and for acquiring fundamental insights into polyploid genome evolution.