Recurrent Urinary tract infections (rUTI) are extremely common, with ~25% of all women who suffer an initial UTI experiencing a recurrence within one year of the original infection. rUTI often occurs when bacteria from the initial infection persist after treatment. Escherichia coli ST131 is a major contributor to hospital and community acquired UTI and is strongly associated with limited treatment options and high rates of recurrence. Here using both high throughput and long read sequencing we examine the stability and dynamics of an E. coli ST131 population isolated over a 5-year period (2012-2016) from the urine and feces of a single individual (patient #1), and elderly women with rUTI since the 1970s. Our data shows that ST131 isolates from patient #1 are highly similar at the core genome level and represent an indigenous clonal lineage specific to this one individual. Remarkably, we identified a stable but highly heterogeneous population persisting in the fecal flora, providing compelling evidence of an intestinal reservoir as a source of rUTI. We show that antibiotic resistant and sensitive intestinal isolates coexist despite frequent challenge with antibiotics, suggesting a population-wide resistance mechanism enabling rapid adaptation to fluctuating environmental antibiotic concentrations. Finally, we describe a remarkably high level of plasmid diversity within ST131 isolates from patient #1 which contributes to strain heterogeneity and show that the loss of a single plasmid dramatically changes the methylation landscape, suggesting the potential for plasmid-dependent regulation of chromosomally encoded methyltransferases. This longitudinal study provides the first comprehensive, in vivo, genomic analysis of a rUTI in a single individual and provides new insight towards understanding the composition and evolution of bacterial populations in a chronic long-term infection.