Adaptation to life in caves is often accompanied by dramatically convergent changes across distantly related taxa, epitomized by the loss or reduction of eyes and pigmentation. Nevertheless, the genomic underpinnings underlying cave-related phenotypes are largely unexplored from a macroevolutionary perspective. Here we investigate genome-wide gene evolutionary dynamics in three distantly related beetle tribes with at least six instances of independent colonization of subterranean habitats, inhabiting both aquatic and terrestrial underground systems. Our results indicate that remarkable gene repertoire changes mainly driven by gene family expansions occurred prior to underground colonization in the three tribes, suggesting that genomic exaptation may have facilitated a strict subterranean lifestyle parallelly across beetle lineages. The three tribes experienced both parallel and convergent changes in the evolutionary dynamics of their gene repertoires. These findings pave the way towards a deeper understanding of the evolution of the genomic toolkit in hypogean fauna.