Hymenopteran insects can provide ecosystem services through their pollination that contributes directly to our food security and economy. Identifying common traits that underlie the effectiveness of pollinators can be challenging because of the diversity in their life-histories. For instance, pollinating bees can be broadly categorized as solitary ones that both reproduce and forage or as social ones specialized to foraging that communicate with others. The small carpenter bee (Ceratina calcarata) is a prominent local pollinator that lives first as a solitary forager and reproducer. It later continues to forage, but in a social nest where it communicates with its adult daughters. Analysis of its brain may therefore reveal common neurological characteristics of pollinating bees as well as differences underlying the behavior of solitary and social bees. Here, we describe a single-nucleus transcriptomic brain atlas of Ceratina calcarata females integrated from adults undergoing diapause in Winter and ones that reproduce and forage in Summer before becoming social. Like other insects, we identify hemocytes, five types of glia, and various types of neurons. Genes upregulated in Summer in neurons, like Kenyon cells, are enriched for processes related to foraging, whereas those genes in glia, like astrocytes, are enriched for reproduction. Because the Kenyon cells and astrocytes show high transcriptionally similarity to those of social insects, the brain architecture of solitary and social C. calcarata foragers seems to be similar despite their behavioral differences. Future comparisons to the brains of pollinators from other species across levels of social organization will clarify the relative roles of phylogeny and life history trait evolution on neurodevelopment and gene expression at the cellular level.