Plasma cells (PC) are terminally differentiated, post-mitotic B-lineage cells that specifically secrete antibodies on a ‘one cell, one specificity’ basis. Once generated, PC migrate to survival niches that occur throughout the body but are concentrated in the bone marrow, and which are considered finite in number. New PC are thought to populate the niches by displacing existing ones such that the majority are constantly turned over, and only a small fraction embedded for prolonged periods. Here, using a novel PC timestamping system, we show that PC can be demarcated into subsets with different survival potential using surface expression of B220 and SLAMF6. New PC are ‘double positive’ (B220+ SLAMF6+) and transition towards a ‘double negative’ (B220-SLAMF6-) compartment that accumulates over time. Using thymidine analogue incorporation, we confirm that ‘double positive’ PC are directly derived from proliferating precursors and have relatively shorter lifespans compared to the non-proliferating ‘double negative’ population. We further demonstrate that this ‘double negative’ population has increased survival potential following ablative irradiation treatments. These data indicate that PC are heterogeneous in survival potential and subsets with increased survival increasingly dominate bone marrow over time. Together these data partition PC based on survival potential, suggesting that access to PC survival niches may become increasingly limited as time progresses. This has implications for vaccine efficacy in mounting a durable memory response and ablative therapies targeting PC neoplasms.