Formerly considered nonfunctional “junk DNA,” pseudogenes have been re-evaluated in light of technological advances in bioinformatics and high-throughput sequencing. The limited research to date on pseudogenes in hexaploid common wheat (Triticum aestivum L.) is largely confined to individual gene families, thus hindering our understanding of the long-term evolutionary dynamics among the A, B, and D subgenomes. Using the IWGSC RefSeq v2.1 genome assembly, we performed genome-wide identification, classification, and analysis of pseudogenes in wheat, including their distribution, evolutionary history, and parental gene functions. Marked asymmetries in pseudogene abundance, distribution, evolutionary dynamics, and constraints were detected among the subgenomes. The B subgenome harbored significantly more pseudogenes and showed distinct evolutionary patterns compared with the A and D subgenomes. Pseudogenes were strongly associated with transposable elements and peaks in their formation were incongruent with ancient genomic upheavals of wheat ancestral lineages. The parent genes were predominantly enriched in non-core functions and showed tissue-specific expression. The findings provide direct evidence for long-term asymmetric, post-polyploidization evolution in wheat, enhance our understanding of polyploid genome evolution, and offer a methodological framework for research on other genetically complex polyploid crops.