Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as an exception. This phylum has been commonly thought to follow two contrasting models of either in situ “mineralization of extracellular matrix” attributed to hyaline rotaliid shells, or “mineralization within intracellular vesicles” attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We found that both groups produced calcareous shells via the intravesicular formation of unstable mineral precursors (Mg-rich amorphous calcium carbonates) supplied by endocytosed seawater and deposited at the site of new wall formation within the organic matrix. Precipitation of high-Mg calcitic mesocrystals took place in situ and formed a dense, chaotic meshwork of needle-like crystallites. We did not observe deposition of calcified needles that had already precipitated in the transported vesicles, which challenges the previous model of miliolid mineralization. Hence, Foraminifera utilize less divergent calcification pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls are therefore apparently created by accumulating and assembling particles of pre-formed liquid amorphous mineral phase within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well-conserved in two clades that represent different chamber formation modes.