The intestinal immune system must balance tolerance to commensal microbes and dietary antigens with protective inflammatory responses to pathogens. This balance is set by antigen-presenting cells (APCs), which acquire luminal antigen and deliver the cytokine and co-stimulatory cues that promote the differentiation of naïve CD4+ T cells into distinct subsets from peripheral regulatory T cells to TH1, TH2 and TH17 effectors. The intestinal APC compartment is correspondingly heterogeneous, comprising multiple dendritic cell (DC) and Thetis cell (TC) subsets alongside monocytes and macrophages. Whether each APC subset has unique roles in regulating CD4 T cell fate is a central question in mucosal immunology. Precise genetic tools are key to addressing this question. However, to date, APC heterogeneity and the subset specific nature of different Cre-drivers have been benchmarked largely in spleen. To determine the full spectrum of intestinal APC heterogeneity and their developmental origin, we performed single-cell RNA sequencing on APCs sorted from Zbtb46, Clec9a and Ms4a3 fate-mapping mice, mapping the labelled and unlabeled compartment of each model onto the full spectrum of intestinal APC states. Surprisingly, we found that lineage tracing did not partition along the anticipated ontogenetic boundaries. Beyond this finding, the resulting atlas provides insights into candidate markers and intersectional strategies for genetic models that resolve intestinal DC, monocyte and macrophage subsets with greater precision facilitating future studies defining how each APC subset contributes to intestinal immunity.