We show that two exopolysaccharide overproducing Tn5 mutants of Rhizobium meliloti, exoR and exoS, have distinct symbiotic defects. While the exoR mutant is unable to colonize nodules, the exoS mutant retains that ability but varies in its ability to produce nitrogen-fixing nodules. We correlate these defects with different degrees of exopolysaccharide overproduction and growth impairment. We further show that the exoR mutant is able to enter developing infection threads but is unable to invade nodule cells. The exoR mutant gives rise to spontaneous pseudorevertants containing second-site suppressor mutations that decrease exopolysaccharide synthesis. These pseudorevertants form nitrogen-fixing nodules. Although the suppressor mutations have the opposite effect on exopolysaccharide production compared to the exoS::Tn5 mutation, they consistently map to the exoS::Tn5 region and belong to the same genetic complementation group as defined by transposon insertion mutations. The effect of the suppressor mutations on exopolysaccharide production is correlated with effects on the expression of exo genes involved in exopolysaccharide synthesis. Finally, we provide evidence that the exoR gene is not required for the regulation of exopolysaccharide synthesis by ammonia.