Spiny projection neurons (SPNs) in the mouse striatum transform multimodal inputs from the cortex and thalamus into inhibitory outputs that regulate basal ganglia activity. SPNs are typically classified into major populations according to their output projection targets and their location within striatal anatomical and neurochemical domains. However, how the cellular and circuit diversity within these broad populations is established developmentally remains largely unknown. We have previously shown that SPNs derived from a distinct apical intermediate progenitor (aIP) pool are preferentially driven by medial prefrontal cortex compared to SPNs derived from other progenitors (OPs), suggesting a role for embryonic progenitors in establishing circuit diversity (van Heusden et al. 2021). Here, we extend these observations by further comparing the cellular identity and synaptic connectivity of aIP and OP-derived SPNs. We first find that aIP-derived SPNs have similar electrophysiological properties but exhibit a greater dendritic complexity. Using ‘patch-seq’, we then find that aIP-derived SPNs are enriched for a specific Nnat+ SPN subtype compared to OP-derived SPNs. Next, with optogenetic and viral circuit mapping approaches we demonstrate that the synaptic connectivity of SPNs reflects progenitor origin, with aIP-derived SPNs receiving a differential excitatory drive from thalamus. Finally, we use single-cell RNA-seq of thousands of aIP and OP-derived SPNs during striatal neural circuit assembly and identify putative regulators of their functional maturation. In conclusion, we provide evidence from several complementary approaches that the fine-scale cellular and circuit diversity of SPNs within the postnatal striatum is generated by distinct embryonic progenitor pools.