Mafb and c-Maf transcription factor (TF) expression is enriched in medial ganglionic eminence (MGE) lineages, beginning in late-secondary progenitors and continuing into mature parvalbumin (PV+) and somatostatin (SST+) interneurons. However, the functions of Maf TFs in MGE development remain to be elucidated. Herein, Mafb and c-Maf were conditionally deleted, alone and together, in the MGE and its lineages. Analyses of Maf mutant mice revealed redundant functions of Mafb and c-Maf in secondary MGE progenitors, where they repress the generation of SST+ cortical and hippocampal interneurons. By contrast, Mafb and c-Maf have distinct roles in postnatal cortical interneuron (CIN) morphological maturation, synaptogenesis, and cortical circuit integration. Thus, Mafb and c-Maf have redundant and opposing functions at different steps in CIN development. Display omitted •Mafb and c-Maf are expressed in MGE-derived CINs but not projection neurons•Mafb and c-Maf control the numbers of MGE-lineage CINs•Loss of Mafb and c-Maf leads to increased SST+ CIN perinatally•Mafb and c-Maf control CIN synaptic maturation antagonistically Using mouse genetics and ex vivo physiology studies, Pai et al. show that Mafb and c-Maf together are necessary to generate the proper numbers of parvalbumin and somatostatin GABAergic interneurons. However, in maturing interneurons, Mafb and c-Maf function divergently to control their firing properties and communication with other neurons.