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<i>Streptococcus agalactiae</i> or group B streptococcus (GBS) is a leading cause of neonatal sepsis and increasingly found as an invasive pathogen in older patient populations. Beta-lactam antibiotics remain the most effective therapeutic with resistance rarely reported, while the majority of GBS isolates carry the tetracycline resistance gene <i>tet(M)</i> in fixed genomic positions amongst five predominant clonal clades. In the UK, GBS resistance to clindamycin and erythromycin has increased from 3% in 1991 to 11.9% (clindamycin) and 20.2% (erythromycin), as reported in this study. Here, a systematic investigation of antimicrobial resistance genomic content sought to fully characterise the associated mobile genetic elements within phenotypically resistant GBS isolates from 193 invasive and non-invasive infections of UK adult patients collected during 2014 and 2015. Resistance to erythromycin and clindamycin was mediated by <i>erm(A)</i> (16/193, 8.2%), <i>erm(B)</i> (16/193, 8.2%), <i>mef(A)</i>/<i>msr(D)</i> (10/193, 5.1%), <i>lsa(C)</i> (3/193, 1.5%), <i>lnu(C)</i> (1/193, 0.5%), and <i>erm(T)</i> (1/193, 0.5%) genes. The integrative conjugative elements (ICEs) carrying these genes were occasionally found in combination with high gentamicin resistance mediating genes <i>aac</i>(6′)<i>-aph</i>(2″), aminoglycoside resistance genes (<i>ant</i>(6-Ia), <i>aph</i>(3′-III), and/or <i>aad(E)</i>), alternative tetracycline resistance genes (<i>tet(O)</i> and <i>tet(S)</i>), and/or chloramphenicol resistance gene <i>cat(Q)</i>, mediating resistance to multiple classes of antibiotics. This study provides evidence of the retention of previously reported ICESag37 (<i>n</i> = 4), ICESag236 (<i>n</i> = 2), and ICESpy009 (<i>n</i> = 3), as well as the definition of sixteen novel ICEs and three novel transposons within the GBS lineage, with no evidence of horizontal transfer.