Gibbons (family Hylobatidae), small apes closely related to humans and great apes, remain understudied despite their threatened status. Here, we present extensive genomic resources, including chromosome-level reference genomes, whole-genome resequencing of 18 extant species, and mitochondrial genomes from 3 ancient samples. Using whole-genome alignments, we resolve the debated phylogeny of the four genera as (Hylobates, (Nomascus, (Symphalangus, Hoolock))). Phylogenetic analyses based on the ancient mitogenomes place the extinct junzi imperialis within Nomascus, refuting its status as a distinct genus. Conservation genomics and ecological niche modeling analyses suggest historical dynamics in gibbon population size and habitat suitability, which are consistent with the potential impacts of past climate change. Through comparative genomics and transgenic mouse experiments, we identify a 205-bp deletion in the Sonic Hedgehog (SHH) gene associated with gibbons' elongated limbs. These findings advance understanding of gibbon evolution, biology, and conservation.