ABSTRACTThe monarch butterfly epitomizes insect biodiversity decline. Understanding the genetic basis of the adaptation of the monarch to a changing environment requires genomic and transcriptomic resources that better reflect its genetic diversity while being informative about gene functionality during life cycle. We report a reference-quality genome assembly from an individual resident at a nonmigratory colony in Mexico, and a new gene annotation and expression atlas for 14,865 genes, including 492 unreported long noncoding RNA (lncRNA) genes, based on RNA-seq data from 14 larval and pupal stages, plus adult morphological sections. Two thirds of the genes show significant expression changes associated with a life stage or section, with lncRNAs being more finely regulated during adulthood than protein-coding genes, and male-biased expression being four times more common than female-biased. The two portions of the heterochromosomeZdisplay distinct patterns of differential expression between the sexes, reflecting that dosage compensation is either absent or incomplete –depending on the sample– in the ancestral but not in the novel portion of theZ. This study represents a major advance in the genomic and transcriptome resources available forD. plexippuswhile providing the first systematic analysis of its transcriptional program across most of its life cycle.