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Oceanic archipelagos comprise multiple disparate environments over small geographic areas and are isolated from other biotas. These conditions have led to some of the most spectacular adaptive radiations, which have been key to our understanding of evolution, and offer a unique chance to characterise the genomic basis underlying rapid and pronounced phenotypic changes. Repeated patterns of evolutionary change in plants on oceanic archipelagos, i.e. the plant island syndrome, include changes in leaf morphology, acquisition of perennial life-style, and change of ploidy. Here, we describe the genome of the critically endangered and Galápagos endemic Scalesia atractyloides Arnot., obtaining a chromosome-resolved 3.2-Gbp assembly with 43,093 candidate gene models. Using a combination of fossil transposable elements, k-mer spectra analyses and orthologue assignment, we identify the two ancestral subgenomes and date their divergence and the polyploidization event, concluding that the ancestor of all Scalesia species on the Galápagos was an allotetraploid. There are a comparable number of genes and transposable elements across the two subgenomes, and while their synteny has been mostly conserved, we find multiple inversions that may have facilitated adaptation. We identify clear signatures of selection across genes associated with vascular development, life-growth, adaptation to salinity and changes in flowering time, thus finding compelling evidence for a genomic basis of island syndrome in Darwin’s giant daisy radiation. This work advances understanding of factors influencing subgenome divergence in polyploid genomes, and characterizes the quick and pronounced genomic changes in a specular and diverse radiation of an iconic island plant radiation.