After being fixed in a population, duplicate genes continuously diverge and diversify in different lineages. Duplicate gene diversification impacts gene network evolution, as well as organismal traits. Here we demonstrate that ongoing diversification of two duplicate gene pairs from the whole genome duplication shaped different network architectures and resulted in different parameters for galactose metabolism. We functionally compared the GALactose utilization networks between Saccharomyces cerevisiae (Scer) and Saccharomyces uvarum (Suva) and found that the resolution of duplicate fate in this network is ongoing in this genus. The first pair, descended from an ancestral kinase and co-inducer, ScerGAL1 and ScerGAL3, are almost completely subfunctionalized in S. cerevisiae, with ScerGAL1 encoding a kinase with weak co-inducing activity and ScerGAL3 encoding a dedicated co-inducer without kinase activity. However, we found that, in S. uvarum, SuvaGAL1 can largely complement the removal of SuvaGAL3, while SuvaGAL3 encodes an inefficient kinase and a co-inducer. Another duplicate pair, GAL80 and GAL80B, encodes two partially redundant GAL gene repressors in S. uvarum, but GAL80B has been lost in S. cerevisiae. In contrast to the well-established rapid growth of a S. cerevisiae gal80-null mutant in galactose, the S. uvarum gal80-null double mutant (gal80∆ gal80b∆) shows initial rapid growth followed by several hours of temporary growth arrest. Surprisingly, closer examination revealed that the S. cerevisiae gal80∆ mutant also shows a temporary growth arrest, but to a much lesser extent. We found that this arrest is likely caused by overly rapid galactose catabolism, which leads to excessive accumulation of reactive oxygen species. Differences between the severity of growth arrest in S. cerevisiae and S. uvarum can largely be explained by differences at the GAL1 locus. Due to technical limitations in detecting the relatively mild effect in S. cerevisiae, this novel observation was not captured by decades of research. Instead, the evolutionary differences between closely related model species rendered this general phenotype more conspicuous and facilitated its discovery. Further examination of gal80-null mutants of both species in a mixture of galactose and fructose or mannose revealed a stronger growth arrest, which indicates a possibly general metabolic conflict with the rapid co-utilization of galactose with fructose and mannose. Our study provides clear evidence that ongoing differential resolution of GAL gene duplicates shaped metabolic network diversification and revealed novel principles of galactose metabolism that might shed light on tradeoffs in carbon metabolism more broadly.