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Ticks and tick-borne diseases are considered a major challenge for human and animal health in tropical, sub-tropical, and temperate regions of the world. However, only scarce information is available on the characterization of tick species infesting dogs in Pakistan. In this study, we present a comprehensive report on the epidemiological and phylogenetic aspects of ticks infesting dogs in Pakistan using the mitochondrial markers i.e. Cytochrome c oxidase subunit 1 (<i>cox1</i>) and 16S ribosomal RNA (<i>16S rRNA</i>) nucleotide sequences. A total of 300 dogs were examined and 1150 ixodid ticks were collected across central Khyber Pakhtunkhwa, Pakistan. The morpho-molecular characterization of hard ticks revealed the presence of two ixodid tick genera on dogs, i.e., <i>Hyalomma</i> and <i>Rhipicephalus</i>, including six tick species viz. <i>Hyalomma dromedarii</i> (15.9%)<i>, Hyalomma excavatum</i> (3%), <i>Rhipicephalus sanguineus s.l.</i> (41.3%)<i>, Rhipicephalus turanicus s.s.</i> (28.7%), <i>Rhipicephalus haemaphysaloides</i> (10.2%), and <i>Rhipicephalus microplus</i> (2%). The total prevalence of tick infestation in dogs was 61%. The district with the highest tick prevalence rate in dogs was Mardan (14.7%), followed by Peshawar (13%), Swabi (12%), Charsadda (11%), and Malakand (10.3%), respectively. Risk factors analysis indicated that some demographic and host management-associated factors such as host age, breed, exposure to acaricides treatment, and previous tick infestation history were associated with a higher risk of tick infestation on dogs. This is the first molecular report confirming the infestation of <i>Hyalomma</i> and <i>Rhipicephalus</i> tick species in the dog population from the study area. The present study also reported a new tick–host association between <i>Hy. excavatum</i>, <i>Hy. dromedarii</i>, and dogs. Phylogenetic analysis revealed that <i>cox1</i> partial nucleotide sequences of <i>Hy. excavatum</i> in our dataset were 100% identical to similar tick specimens identified in Turkey, and those of <i>Hy. dromedarii</i> were identical to tick specimens from Iran. Whereas, <i>Rh. haemaphysaloides</i> and <i>Rh. microplus’ cox1</i> partial nucleotide sequences were identical to sequences previously published from Pakistan. <i>Rhipicephalus turanicus s.s.</i> ‘s <i>cox1</i> isolates from the present study were 99.8–100% identical to Pakistani-reported isolates, and those of <i>Rh. sanguineus s.l.</i> were 100% identical to Chinese specimens. Results on the genetic characterization of ticks were further confirmed by <i>16S rRNA</i> partial nucleotide sequences analysis, which revealed 100% identity between the tick isolates of this study and those of <i>Hy. excavatum</i> reported from Turkey; <i>Hy. dromedarii</i> specimens reported from Senegal; <i>Rh. haemaphysaloides</i>, <i>Rh. microplus</i>, and <i>Rh. turanicus s.s.</i>, previously published from Pakistan, and <i>Rh. sanguineus s.l.</i>, published from China. Furthermore, phylogenetic analysis showed that the <i>Rh. sanguineus s.l.</i> isolates of this study clustered with specimens of the tropical lineage with 7.7–10% nucleotide divergence from the specimens of the temperate lineage. Further molecular works need to be performed throughout Pakistan to present a more detailed map of tick distribution with information about dog host associations, biological characteristics, and pathogen competence.