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<i>Streptococcus suis</i> causes disease in pigs and is implicated increasingly in human disease worldwide. Although most clinical cases are associated with serotype 2, infections by other serotypes have sometimes been reported. Here, we sequenced the genome of a multidrug-resistant <i>S. suis</i> serotype 28 (strain 11313) and a multidrug-resistant <i>S. suis</i> serotype 31 (strain 11LB5). Strain 11313 was apathogenic in mouse infection models, whereas strain 11LB5 displayed ganglion demyelination, meningeal thickening, congestion, mononuclear cell infiltration, massive proliferation of cortical glial cells, and bacteria (>10⁴ CFU/g) in the spinal cord and ganglia in mice. Furthermore, immunohistochemistry found that the heavily infiltrated glial cells were astrocytes. Strain 11313 harbored the resistance genes <i>ant(6)-Ia</i>, <i>erm(B)</i>, <i>optrA</i>, <i>tet(l)</i>, <i>tet(o)</i>, and strain 11LB5 harbored the resistance genes <i>ant(6)-Ia</i>, <i>erm(B)</i>, <i>tet(40)</i>, <i>tet(o/w/32/o)</i>, <i>aac(6′)-aph(2″)</i>. Mouse studies showed that strain 11LB5 exhibited a similar virulence to serotype 2 strain 700794, highlighting the need for surveillance of the other serotype <i>S. suis</i> isolates, in addition to serotype 2, in farms. This is the first report of the aminoglycoside resistance gene <i>ant(6)-Ia</i> in <i>S. suis</i> from animals. This suggests that <i>S. suis</i> might serve as an antibiotic resistance reservoir, which spreads the resistance gene <i>ant(6)-Ia</i> or <i>optrA</i> to other streptococcal pathogens on farms.