In eukaryotes, genome size correlates little with the number of coding genes or the level of organismal complexity (C-value paradox). The underlying causes of variations in genome size, whether adaptive or neutral, remain unclear, although several biological traits often covary with it 1–5. Rapid increases in genome size occur mainly through whole-genome duplications or bursts in the activity of transposable elements (TEs) 6. The very small and compact genome of Oikopleura dioica, a tunicate of the larvacean class, lacks elements of most ancient families of animal retrotransposons 7, 8. Here, we sequenced the genomes of six other larvaceans, all of which are larger than that of Oikopleura (up to 12 times) and which increase in size with greater body length. Although no evidence was found for whole-genome duplications within the group of species, the global amount of TEs strongly correlated with genome size. Compared to other metazoans, however, the TE diversity was reduced in all species, as observed previously in O. dioica, suggesting a common ancestor with a compacted genome. Strikingly, non-autonomous elements, particularly short interspersed nuclear elements (SINEs), massively contributed to genome size variation through species-specific independent amplifications, ranging from 3% in the smallest genome up to 49% in the largest. Variations in SINE abundance explain as much as 83% of interspecific genome size variation. These data support an indirect influence of autonomous TEs on genome size via their ability to mobilize non-autonomous elements. Display omitted •Genome size varies up to 12× in larvaceans, chordates with a distinctive anatomy•Small and large species have the smallest and largest genomes, respectively•Transposable elements have driven multiple independent genome expansions•Genomes mainly increased through accumulations of non-autonomous elements (SINEs) The causes of genome size variation and their relation with life traits are poorly understood. Naville, Henriet, et al. show that, in tunicate larvaceans, close relatives of vertebrates, multiplications of non-autonomous transposable elements were the main drive of remarkable genome expansions.