Morphogenesis of the mammalian kidney requires reciprocal interactions between two cellular domains at the periphery of the developing organ: the tips of the epithelial ureteric tree and adjacent regions of cap mesenchyme. While the presence of the cap mesenchyme is essential for ureteric branching, how the cap mesenchyme is specifically maintained at the tips is unclear. In addition, while lineage tracing shows that cap mesenchyme cells commit to form the epithelial nephrons, how this fate change is effected within the niche and how the balance of turnover versus exit is regulated is not understood. Using ex vivo timelapse imaging across 18 hours of developing mouse kidney, we show that cells of the cap mesenchyme are highly motile. Individual cap mesenchyme cells move within and between cap domains. Individual tracks collected for >800 cells showed evidence that this movement was largely stochastic, with cell autonomous migration influenced by opposing attractive, repulsive and cell adhesion cues. These competing forces facilitate the dynamic remodelling required to maintain a domain around the ureteric tips, which is vital for continued branching and nephron induction. Continuous cell movement within the cap mesenchyme results in a constant change in the signalling environment of any given cell. While the signal for this change in cell identity has been regarded as coming from the tip, how a motile population is triggered to change fate is unclear. Wnt4 is regarded as a marker of commitment. Using tamoxifen-induced Wnt4-Cre labelling, we have observed that a small proportion of cells trigger Wnt4 expression but remain uncommitted, remaining motile within the cap mesenchyme. As a result of repeated accumulation of such cells, the cap mesenchyme population is altered across developmental time, potentially resulting in the eventual loss of capacity to drive further branching. These studies reveal a highly dynamic environment where stochastic decisions at the level of the individual cell result at the organ level in highly reproducible form.