Plant height, petiole length, and the angle of the leaf petiole and branch angles are crucial traits determining plant architecture and yield in soybean (Glycine maxL.). Here, we characterized a soybean mutant with super-short petioles (SSP) and enlarged petiole angles (namedGmssp) through phenotypic observation, anatomical structure analysis, and bulk sequencing analysis. To identify the gene responsible for theGmsspmutant phenotype, we established a pipeline involving bulk sequencing, variant calling, functional annotation by SnpEFF (v4.0e) software, and Integrative Genomics Viewer analysis, and we initially identifiedGlyma.11G026400, encoding a homolog of Anaphase-promoting complex subunit 8 (APC8). Another mutant,t7, with a large deletion of many genes includingGlyma.11G026400, has super-short petioles and an enlarged petiole angle, similar to theGmsspphenotype. Characterization of thet7mutant together with quantitative trait locus mapping and allelic variation analysis confirmedGlyma.11G026400as the gene involved in theGmsspphenotype. InGmssp, a 4 bp deletion inGlyma.11G026400leads to a 380 aa truncated protein due to a premature stop codon. The dysfunction or absence ofGlyma.11G026400caused severe defects in morphology, anatomical structure, and physiological traits. Transcriptome analysis and weighted gene co-expression network analysis revealed multiple pathways likely involved in these phenotypes, including ubiquitin-mediated proteolysis and gibberellin-mediated pathways. Our results demonstrate that dysfunction ofGlyma.11G026400leads to diverse functional consequences in different tissues, indicating that this APC8 homolog plays key roles in cell differentiation and elongation in a tissue-specific manner. Deciphering the molecular control of petiole length and angle enriches our knowledge of the molecular network regulating plant architecture in soybean and should facilitate the breeding of high-yielding soybean cultivars with compact plant architecture.