During infectious disease outbreak investigations, mutation rates amongst lineages of clinical bacterial pathogens can be highly variable; what is classified as multiple outbreaks could indicate high genetic variation amongst descendants of a single outbreak event. Consequently, the best way to define the genetic boundaries of an outbreak cluster is currently unclear. Over 2720 generations of mutation accumulation on average, I explored mutation rate and fitness decline variation in nine clinical isolates of Escherichia coli and I found that there was high variation between, but less commonly within, genotypes. Genotypes could be generally be categorised by mutation rate and fitness decline variation between replicates as either: (1) non-mutator genotypes with low variation, non-mutator genotypes with high variation because of (2) (an) infrequent mutator replicate(s), or (3) mutator genotypes with high or low variation. My findings have important implications both for molecular epidemiology of bacterial pathogens and predicting evolution in pathogen pathways.