True morels (Morchella, Pezizales) are a popular edible and medicinal fungus with great nutritional and economic value. The dynamics and regulatory mechanisms during the morphogenesis and maturation of morels are poorly understood. In this study, the metabolomes and transcriptomes of the mycelium (MY), primordium differentiation (PR), young fruiting body (YFB), and mature fruiting body (MFB) were comprehensively analyzed to reveal the mechanism of the morphogenesis and maturation of Morchella sextelata. A total of 748 differentially expressed metabolites (DEMs) and 5342 differentially expressed genes (DEGs) were detected, mainly enriched in the carbohydrate, amino acid, and lipid metabolism pathways, with the transition from the mycelium to the primordium being the most drastic stage at both the metabolic and transcriptional levels. The integrated metabolomics and transcriptomics highlighted significant correlations between the DEMs and DEGs, and specific amino acid and nucleotide metabolic pathways were significantly co-enriched, which may play key roles in morphological development and ascocarp maturation. A conceptual model of transcriptional and metabolic regulation was proposed during morphogenesis and maturation in M. sextelata for the first time, in which environmental factors activate the regulation of transcription factors, which then promote metabolic and transcriptional regulation from vegetative to reproductive growth. These results provide insights into the metabolic dynamics and transcriptional regulation during the morphogenesis and maturation of morels and valuable resources for future breeding enhancement and sustainable artificial cultivation.