There is considerable interest in harnessing bacterial catabolic activities to valorize lignin-derived compounds. One such class of compounds, hydroxyphenylethanones (HPEs), includes acetovanillone (AV), 4-hydroxyacetophenone (HAP), and acetosyringone (AS). Despite occurring in various industrial streams of lignin, there are few reports on their microbiological degradation. Here, we report that Rhodococcus aromaticirovans RHA1 cometabolizes, but does not grow on, AV and HAP, converting them to 3,4-dihydroxyacetophenone (3,4-DHAP), a catechol with pharmacological properties. Molecular genetics studies revealed that AgcAB, a cytochrome P450 alkylguaiacol O-demethylase, catalyzes AV O-demethylation and AphAB, an alkylphenol hydroxylase, catalyzes HAP hydroxylation. Additionally, AV induced the expression of AgcA and the alkylcatechol extradiol dioxygenase, AphC. The specificity (kcat/KM) of AgcAB for AV was ~7% that of 4-propylguaiacol, while AphC cleaved 3,4-DHAP at ~8% the rate of 4-methylcatechol. We also compared the activity of HPE catabolic pathways from three strains by integrating their genes into RHA1. In resting cell assays, a strain expressing the hpe genes of Rhodococcus rhodochrous GD02 converted AV 43- and 97-fold faster than strains expressing pathways from Actinomadura macra sp. NBRC-14102 and Sphingobium lignivorans SYK-6, respectively. All three pathways preferentially converted AV and HAP over AS. However, the strain expressing the SYK-6 pathway had the highest relative activity for AS, 18% its activity on AV. The GD02 hpe genes enabled the growth of RHA1 on HPEs, and it grew faster on AV than on GD02. Overall, this work provides insight into the substrate preference of aromatic catabolic enzymes, highlights the value of cometabolism for biocatalysis, and facilitates the engineering of microbial cell factories to valorize HPEs.