Airbreathing catfishes (clariids) are a group of stenohaline freshwater fish that can withstand various environmental conditions and farming practices, including the ability to breathe atmospheric oxygen. This unique ability has allowed them to thrive in semi-terrestrial habitats. However, the underlying genomic and adaptive mechanisms remain poorly investigated. Here, we sequenced the genome of the African catfish Clarias gariepinus, one of the most commonly farmed clariids, and generated a gapless telomere-to-telomere (T2T) chromosome-level assembly with high-resolution haplotypes, by integrating long-range sequencing (Hi-C) with PacBio single-molecule (HiFi), Oxford Nanopore, and Illumina sequencing data. The diploid genome assembly yielded 58 contigs with a total length of 969.72 Mb and a contig N50 of 33.71 Mb. We report 25,655 predicted protein-coding genes and 49.94% repetitive elements in the African catfish genome. Our genome assembly provides the first comprehensive gene annotation and haplotype information, such as the male-specific haplotype, enabling us to identify putative genes and molecular mechanisms underlying amphibious traits and terrestrial adaptation of airbreathing catfishes. Several gene families involved in ion transport, osmoregulation, oxidative stress response, and muscle metabolism were expanded or positively selected in clariids, suggesting a potential role in their transition to terrestrial life. The reported findings expand our understanding of the genomic mechanisms underpinning the resilience and adaptive mechanisms of C. gariepinus to adverse ecological conditions. They will serve as a valuable resource for future studies in elucidating these unique biological traits in related teleosts and leverage these insights for aquaculture improvement.