Comprehensive transcriptomic survey of the pig (Sus scrofa) may lead to a better understanding of mechanisms of tissue specialization that underlie economic traits of this species and accelerate its use as a biomedical model. Here, we characterized four distinct transcript types (lncRNAs, TUCPs, miRNAs and circRNAs) in 31 adult pig tissues and two cell lines, together with protein-coding genes. We dissected their distinct structural and transcriptional features and uncovered transcriptome variability as related to tissue physiology. We discovered extraordinary diversity among 47 anatomically distinct skeletal muscle types, as well as among six adipose depots, which are linked to their diverse origins, metabolic features, cell composition, physical activity and mitochondrial pathways. In particular, transcription of HOX genes across skeletal muscles exhibited a position-dominant pattern, revealing a similar developmental history of these tissues within the same body part. Transcriptional patterns across adipose depots demonstrated a metabolically protective role of subcutaneous adipose tissue and the association of visceral adipose tissue with metabolic dysfunction. Comparative analysis of the transcriptomes of seven tissues of the pig and nine other vertebrates revealed insights into evolutionary divergence of transcription that contributes to lineage-specific tissue biology. We also analyzed long-range regulation of promoters by their enhancers with downstream transcription in subcutaneous adipose tissues of six mammals, showing that evolutionary stability of transcription can mainly be attributed to multiple enhancers buffering gene expression patterns against genetic perturbations, thereby conferring robustness during speciation. Collectively, this study offers a resource for the accelerated use of the pig as a biomedical model for human biology and disease and uncovers molecular bases of its diverse economic traits.