Midbrain dopaminergic (mDA) neurons in the substantia nigra are selectively degenerated in Parkinson’s disease (PD), leading to motor deficits and a broad range of non-motor symptoms. As no curative treatment currently exists for PD, cell replacement therapy involving the transplantation of dopaminergic neuron precursors into patient brains represents a promising mode of treatment. Several studies have shown a range of transcriptional subtypes that exist among mDA neurons, with implications for their eventual axonal targets and synaptic function. Grafts that contain contaminating cell types such as serotonergic neurons may lead to off-target effects and reduce treatment efficacy. Using midbrain-like organoids (MLOs) derived from human pluripotent stem cells, we define major cell types of the midbrain and delineate its developmental trajectories using single cell transcriptomics. We compare these developmental programs to the fetal midbrain and show that MLOs are able to recapitulate the cell type diversity of the midbrain seen in vivo, and are transcriptionally similar to their age-matched counterparts in the fetal brain. We also note the appearance of the A9-like dopaminergic neuronal population affected in PD, which becomes functionally mature within 6 months in culture. Through our analysis, we identify transcriptional programs that are upregulated in dopaminergic precursors. Furthermore, we transplanted dopaminergic neuron precursors derived from MLOs into substantia nigra-lesioned mice models, showing that MLOs have therapeutic potential to correct motor deficits in a mouse model of PD. These results can be used to guide stem-cell therapies of PD, and produce better quality grafts of dopaminergic neuronal progenitors.