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Hard ticks (Ixodida: Ixodidae) are medically important ectoparasites that feed on all classes of terrestrial vertebrates. Recently, we molecularly characterized hard ticks and associated <i>Anaplasma</i> spp. in the northern and central regions of Khyber Pakhtunkhwa (KP), Pakistan; however, this knowledge was missing in the southern regions. This study aimed to investigate tick prevalence, host range, genetic diversity, and molecular survey of <i>Anaplasma</i> spp. in a wide range of tick species in two distinct physiographic regions of southern KP. A total of 1873 hard ticks were randomly collected from 443/837 hosts (cattle, Asian water buffaloes, horses, goats, sheep, dogs, and camels) in Lakki Marwat, Bannu, and Orakzai districts of KP. Overall, 12 tick species were morphologically identified, among which <i>Hyalomma dromedarii</i> was the most prevalent species (390/1873, 20.9%), followed by <i>Hy. anatolicum</i> (294, 15.7%), <i>Rhipicephalus microplus</i> (262, 14%), <i>Hy. scupense</i> (207, 11.1%), <i>R. sanguineus</i> (136, 7.3%), <i>R. turanicus</i> (121, 6.5%), <i>Haemaphysalis cornupunctata</i> (107, 5.7%), <i>R. haemaphysaloides</i> (110, 5.9%), <i>Ha. montgomeryi</i> (87, 4.6%), <i>Hy. isaaci</i> (58, 3.1%), <i>Ha. bispinosa</i> (54, 2.9%), and <i>Ha. sulcata</i> (47, 2.5%). The extracted DNA from a subset of each tick species was subjected to PCR to amplify <i>cox1</i> or <i>16S rRNA</i> sequences of ticks and <i>16S rRNA</i> sequences of <i>Anaplasma</i> spp. The tick <i>cox1</i> sequences showed 99–100% identities with the sequences of the same species, whereas <i>16S rRNA</i> sequences of <i>R. turanicus</i>, <i>Ha. montgomeryi</i> and <i>Ha. sulcata</i> showed 97–100% identities with the corresponding species. The <i>16S rRNA</i> sequence of <i>Ha. cornupunctata</i> showed 92% identity with the species from the same subgenus, such as <i>Ha. punctata</i>. The <i>16S rRNA</i> sequence of <i>Anaplasma</i> spp. showed 100% identity with <i>Anaplasma marginale</i>. Moreover, 54 ticks were found positive for <i>A. marginale</i> with a total infection rate of 17.2%. The highest infection rate was recorded in <i>Hy. dromedarii</i> (31.1%) and the lowest in each <i>R. haemaphysaloides</i> and <i>R. sanguineus</i> (20%). All the <i>cox1</i> or <i>16S rRNA</i> sequences in phylogenetic trees clustered with the same species, except <i>Ha. cornupunctata</i>, which clustered with the <i>Ha</i>. (<i>Aboimisalis</i>) <i>punctata</i>. In this study, <i>Ha. cornupunctata</i> was reported for the first time at the molecular level. The genetic characterization of ixodid ticks and molecular detection of associated <i>A. marginale</i> will assist in the epidemiological surveillance of these parasites in the region.