Giant genomes, generally dominated by transposable elements (TEs), have evolved repeatedly in angiosperms. The role of TEs in the evolution of giant genomes, however, remains largely unclear. Here, by ancestral genome size reconstruction, whole-genome sequencing, and comparative genomic and transcriptomic analyses, we reveal the processes, drivers, and consequences of genomic gigantism in the buttercup family (Ranunculaceae). We find that the giant diploid genome of Nigella damascena (10.84 Gb, ~35 times that of columbine) has evolved from an ~1.46 Gb ancestral genome by persistent TE accumulation over 60 million years. TE insertions in genic regions have generated genes with ultra-long introns or altered coding sequences, as well as Nigella-specific TE-derived genes, collectively accounting for ~20% of protein-coding genes in the N. damascena genome. TE-mediated regulatory changes and gene duplications/losses likely underpin the evolution of elaborate petals, fused carpels, and specialized secondary metabolites in N. damascena. These findings reveal how TEs drive genomic gigantism and shape specialized traits, advancing our understanding of genome size evolution.