Single-cell (sc)RNA-seq, together with RNA velocity and metabolic labeling, reveals cellular states and transitions at unprecedented resolution. Fully exploiting these data, however, requires kinetic models capable of unveiling governing regulatory functions. Here, we introduce an analytical framework dynamo (https://github.com/aristoteleo/dynamo-release), which infers absolute RNA velocity, reconstructs continuous vector fields that predict cell fates, employs differential geometry to extract underlying regulations, and ultimately predicts optimal reprogramming paths and perturbation outcomes. We highlight dynamo 's power to overcome fundamental limitations of conventional splicing-based RNA velocity analyses to enable accurate velocity estimations on a metabolically labeled human hematopoiesis scRNA-seq dataset. Furthermore, differential geometry analyses reveal mechanisms driving early megakaryocyte appearance and elucidate asymmetrical regulation within the PU.1-GATA1 circuit. Leveraging the least-action-path method, dynamo accurately predicts drivers of numerous hematopoietic transitions. Finally, in silico perturbations predict cell-fate diversions induced by gene perturbations. Dynamo , thus, represents an important step in advancing quantitative and predictive theories of cell-state transitions. [Display omitted] • Modeling time-resolved scRNA-seq data avoids pitfalls of splicing RNA velocities • Dynamo reconstructs analytical vector fields from discrete velocity vectors • Vector fields reveal the timing and mechanisms of human hematopoiesis • Dynamo allows cell-state transition path and in silico perturbation predictions Dynamo is a computational framework for gaining insights into dynamic biological processes, such as human hematopoiesis, from time-resolved single-cell RNA-seq data. Dynamo constructs transcriptomic vector fields from single-cell data and enables predictive modeling of cell-state regulatory mechanisms, perturbation outcomes, and optimal paths for cell-state transitions. [ABSTRACT FROM AUTHOR]