Plastic recycling is currently limited by the high cost of sorting and breakdown and the low market value of the end products. Here, we present a hybrid chemical-biological process to convert dirty plastic waste into nutritionally enriched microbial biomass. Post-consumer high- and low-density polyethylene (HDPE/LDPE) was converted into mixed dicarboxylic acids (DCAs) through accelerated thermal oxidative decomposition (ATOD). The ATOD method was optimized to bias the DCA product distribution for easier consumption by microbes and found to be even compatible with polyethylene terephthalate and polystyrene. A library screen comprised of 25 DCA-degrading bacterial species identified A. baylyi as the optimal candidate due to its broad substrate range, rapid growth, metabolic flexibility, scalability, and genetic tractability. A. baylyi was engineered to overexpress the transcription factor CaiB, which improved DCA consumption when used as the sole carbon source and reduced the lag phase during large-scale biomanufacturing. While not classified as a GRAS strain, A. baylyi has been found in the human food supply and could be engineered to produce dietary compounds, proteins, and flavorants. The engineered strain was further modified to convert PE-derived DCAs into riboflavin (vitamin B2) and β-carotene (provitamin A) through the introduction of multi-gene recombinant pathways into the A. baylyi genome. Biomass generated from both the wild-type and engineered A. baylyi strains were assessed for protein, fiber, lipid, heavy metals, RNA, and allergens to build a comprehensive nutritional profile. This work demonstrates the conversion of recalcitrant waste plastic into a nutritious product and a potential food source for animals, including humans.