Pancreas injury by partial duct ligation (PDL) activates a healing response, encompassing β‐cell neogenesis and proliferation. Macrophages (MΦs) were recently shown to promote β‐cell proliferation after PDL, but they remain poorly characterized. We assessed myeloid cell diversity and the factors driving myeloid cell dynamics following acute pancreas injury by PDL. In naive and sham‐operated pancreas, the myeloid cell compartment consisted mainly of two distinct tissue‐resident MΦ types, designated MHC‐IIlo and MHC‐IIhi MΦs, the latter being predominant. MHC‐IIlo and MHC‐IIhi pancreas MΦs differed at the molecular level, with MHC‐IIlo MΦs being more M2‐activated. After PDL, there was an early surge of Ly6Chi monocyte infiltration in the pancreas, followed by a transient MHC‐IIlo MΦ peak and ultimately a restoration of the MHC‐IIhi MΦ‐dominated steady‐state equilibrium. These intricate MΦ dynamics in PDL pancreas depended on monocyte recruitment by C‐C chemokine receptor 2 and macrophage‐colony stimulating factor receptor as well as on macrophage‐colony stimulating factor receptor‐dependent local MΦ proliferation. Functionally, MHC‐IIlo MΦs were more angiogenic. We further demonstrated that, at least in C‐C chemokine receptor 2‐KO mice, tissue MΦs, rather than Ly6Chi monocyte‐derived MΦs, contributed to β‐cell proliferation. Together, our study fully characterizes the MΦ subsets in the pancreas and clarifies the complex dynamics of MΦs after PDL injury.