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Indwelling urinary catheters are common in health care settings and can lead to catheter-associated urinary tract infection (CAUTI). Long-term catheterization causes polymicrobial colonization of the catheter and urine, for which the clinical significance is poorly understood. Through prospective assessment of catheter urine colonization, we identified <i>Enterococcus faecalis</i> and <i>Proteus mirabilis</i> as the most prevalent and persistent co-colonizers. Clinical isolates of both species successfully co-colonized in a murine model of CAUTI, and they were observed to co-localize on catheter biofilms during infection. We further demonstrate that <i>P. mirabilis</i> preferentially adheres to <i>E. faecalis</i> during biofilm formation, and that contact-dependent interactions between <i>E. faecalis</i> and <i>P. mirabilis</i> facilitate establishment of a robust biofilm architecture that enhances antimicrobial resistance for both species. <i>E. faecalis</i> may therefore act as a pioneer species on urinary catheters, establishing an ideal surface for persistent colonization by more traditional pathogens such as <i>P. mirabilis</i>.