The Structural Maintenance of Chromosomes (SMC) complex plays an important role in chromosome organization and segregation in most living organisms. In Caulobacter crescentus, SMC is required to align the left and the right arms of the chromosome that run in parallel down the long axis of the cell. However, the mechanism of SMC-mediated alignment of chromosomal arms remains elusive. Here, using a genome-wide chromosome conformation capture assay, chromatin immunoprecipitation with deep sequencing, and microscopy of single cells, we show that Caulobacter SMC is recruited to the centromeric parS site and that SMC-mediated arm alignment depends on the chromosome partitioning protein ParB. We provide evidence that SMC likely tethers the parS-proximal regions of the chromosomal arms together, promoting arm alignment. Strikingly, the co-orientation of SMC translocation and the transcription of highly-expressed genes is crucial for the alignment of parS-proximal regions of the chromosomal arms. Highly-transcribed genes near parS that are oriented against SMC translocation disrupt arm alignment suggesting that head-on transcription interferes with SMC translocation. Our results demonstrate a tight interdependence of bacterial chromosome organization and global patterns of transcription.