Abstract The Lemnaceae (duckweeds) are the world’s smallest but fastest growing flowering plants, with a drastically reduced morphology and predominant clonal reproductive habit capable of continuous exponential growth. Here, we present assemblies of 10 Lemna chromosome sets by single molecule nanopore sequencing and chromosome conformation capture. Dynamics of genome evolution in the family are revealed by syntenic comparisons with Wolffia and Spirodela , and diversification of these genera was found to coincide with the “Azolla event”, in which blooms of aquatic macrophytes reduced atmospheric CO 2 from greenhouse levels found in the Eocene to those of the current ice age. Orthologous gene comparisons with other aquatic and terrestrial plants uncovered candidate genes for the unique metabolic and developmental features of the family, such as frequent hybrid polyploidy, lack of stomatal closure in high CO 2 , and accumulation of calcium oxalate, a promising candidate for carbon sequestration. Loss of a spermine-triggered gene network may account for drastic reduction in stature and preferentially adaxial stomata, a feature of floating aquatic plants. Strikingly, Lemnaceae genomes have selectively lost some of the genes required for RNA interference, including Argonaute genes required for post-zygotic reproductive isolation (the triploid block) and reduced gamete formation. Triploid hybrids arise commonly among Lemna , presumably by hybridization with unreduced gametes, and we have found mutations in highly-conserved ZMM crossover pathway genes that could support polyploid meiosis. Rapid but stable clonal propagation makes Lemna an ideal platform for continuous protein and starch micro-cropping, and for efficient sequestration of dissolved nutrients and atmospheric CO 2 . Facile regeneration of transgenic fronds from tissue culture, aided by reduced epigenetic silencing, makes Lemna a powerful biotechnological platform, as exemplified by recent engineering of high-oil Lemna that out-perform oil seed crops.