Plasma cells (PC) mediate humoral immunity because they produce antibodies. PC survive for varying periods of time, ranging from a few days to many months, but whether this difference arises stochastically or deterministically is undefined. Here, we have used PC timestamping in mice to show that long-lived PC (LLPC) and short-lived PC are transcriptionally and phenotypically unique. In basic characterisations, PC of all isotypes formed the LL compartment, but a core set of 46 genes was uniquely expressed in 60-day-old PC relative to short-lived PC and this expression was conserved in PC aged 270 days or more. Using this core program, we resolved six distinct PC clusters by single cell sequencing, and validated a molecular phenotype of the PC subset with the slowest decay by flow cytometry. Three molecules distinguished PC that survived for days to weeks from those that survive for 6 months or more, identifying a simple means to characterize PC based on their predicted lifespan. The halflife of the average PC in mice at homeostasis was calculated to be 91 days. We conclude that PC turnover is not a simple stochastic process, but that heterogeneity in PC gene expression profiles causes variation in PC survival. These findings establish the LLPC transcriptome and suggest a core set of genes underlies the extended lifespan of a unique subset of PC.