The sweet potato whitefly, Bemisia tabaci, is a globally important pest that poses serious challenges to agriculture because of its remarkable ability to adapt and thrive in various environments. Despite its widespread presence, its development and growth remain poorly understood. In this study, we used a comprehensive multiomics approach, including small RNA (microRNA (miRNA)) sequencing, messenger RNA (mRNA) transcriptomics, and quantitative proteomics, to decipher the molecular developmental dynamics of B. tabaci at different life stages, such as eggs, nymphs, puparia (pupae), and adults. The findings revealed two principal ontogenetic stages in the life cycle of B. tabaci. The initial phase encompasses ontogenetic metamorphosis from the ovum to the inaugural nymphal instar, characterized by a decrease in matrilineal influence and an increase in metabolic activity. The subsequent phases occur as the organism advances its transition from the fourth-instar nymph stage to sexual maturity, resulting in profound metamorphic transformations and ecological adaptations. We revealed that specific miRNAs, especially Btab-miR-34 and Btab-miR-2944b, play critical roles in regulating these stages by repressing processes such as DNA replication and cuticle formation. Furthermore, novel miRNAs such as bta-miR-307a, bta-miR-352a, and bta-miR-107a have emerged as key regulators that direct pathways involved in detoxification and environmental sensing. Our analysis of transcriptional dynamics revealed that each life stage has a unique molecular blueprint. Eggs focus mainly on replication, whereas adults produce proteins related to detoxification and sensory functions. Proteomic data further confirmed that these molecular programs are functionally active during development. This network suggests that established miRNAs are crucial for maintaining developmental stability, whereas newer regulators support lineage-specific adaptations that improve survival. This research highlights the complex and finely tuned molecular mechanisms that regulate the growth and development of B. tabaci. These insights also offer valuable information that can help improve pest management strategies in agriculture.