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The torque teno sus virus (TTSuV) is an emerging virus threating the <i>Suidae</i> species of unclear pathogenicity, although it was previously reported as a worsening factor of other porcine diseases, in particular, porcine circovirus associated disease (PCVAD). Here, a comprehensive codon usage analysis of the open reading frame 1 (ORF1), which encodes the viral capsid protein, was undertaken for the first time to reveal its evolutionary history. We revealed independent phylogenetic processes for the two genera during TTSuV evolution, which was confirmed by principal component analysis (PCA). A low codon usage bias was observed in different genera and different species, with Kappatorquevirus a (TTSuVk2a) displaying the highest, which was mainly driven by mutation pressure and natural selection, especially natural selection. Overall, ATs were more abundant than GCs, along with more A-ended synonymous codons in relative synonymous codon usage (RSCU) analysis. To further confirm the role of natural selection and TTSuV adaptation to the <i>Suidae</i> species, codon adaptation index (CAI), relative codon deoptimization index (RCDI), and similarity index (SiD) analyses were performed, which showed different adaptations for different TTSuVs. Importantly, we identified a more dominant role of <i>Sus scrofa</i> in the evolution of <i>Iotatorquevirus</i> (TTSuV1), with the highest CAI values and lowest RCDI values compared to <i>Sus scrofa domestica</i>. However, in TTSuVk2, the roles of <i>Sus scrofa</i> and <i>Sus scrofa domestica</i> were the same, regarding codon usage, with similar CAI and RCDI values. Our study provides a new perspective of the evolution of TTSuV and valuable information to develop control measures against TTSuV.