Chemoreceptors and cytoplasmic chemotaxis proteins in Escherichia coli form clusters that play a key role in signal processing. These clusters localize at cell poles and at specific positions along the cell body which correspond to future division sites, but the details of cluster formation and the mechanism of cluster distribution remain unclear. Here, we used fluorescence microscopy to investigate how the numbers and sizes of receptor clusters depend on the expression level of chemotaxis proteins and on the cell length. We show that the average cluster number saturates at high levels of protein expression at approximately 3.7 clusters per cell, well below the number of available positioning sites. Correspondingly, distances between clusters in filamentous cells saturate at an average of 1 μm but, even at saturating expression levels, individual cluster numbers and distances show a broad distribution around the mean. Our data imply a stochastic mode of cluster assembly, where a defined average interval between clusters along the cell body arises from competition between nucleation of new clusters and growth of existing clusters. Upon subsequent anchorage to defined lateral sites, clusters grow with rates that inversely depend on their size, and become polar upon several rounds of cell division.