 Dempsey akatumidzwa kunzvimbo ye2006 FIFA World Cup yeUnited States uye akahwina chibodzwa chega cheAmerica mumakwikwi ese, panguva yekurasikirwa ne21 kuGhana mumutambo wekupedzisira weboka. Akarova zvibodzwa zvitatu pa2009 FIFA Confederations Cup, imwe neimwe ichirwisa Egypt, Spain, neBrazil, uye akabatsira kutungamira United States kuti apedze semumhanyi. Chibodzwa chaDempsey chete panguva ye2010 FIFA World Cup chakauya mukukwikwidza 11 kuenda kuEngland, zvichimuita wechipiri weAmerica kurova mumakwikwi akawanda eWorld Cup. Mumutambo wekuvhura we2014 FIFA World Cup vachipesana neGhana, Dempsey akarova 30 masekondi mushure mekubaya, chibodzwa chechishanu chinokurumidza munhoroondo yeWorld Cup; akazovewo muAmerican wekutanga kurova mumakwikwi matatu akateedzana eWorld Cup. Ndiye akahwina zvibodzwa mu2015 CONCACAF Gold Cup, achihwina zvibodzwa zvinomwe zveUnited States panguva yekukunda kwavo mumakwikwi uye achiisa rekodhi yezvinangwa zvakawanda zvakaitwa nemuAmerican paGold Cup. Musi waChikunguru 22, 2017, panguva ye2017 CONCACAF Goridhe Mukombe semifinal vachipesana neCosta Rica, Dempsey akaenzana naLandon Donovan rekodhi yemutambi wepamusoro wenguva dzese nechinangwa chake che57. Donovan pachake akadana zvinyorwa zvaDempsey zvinoshamisa zvikuru, achiwedzera kuti Dempsey akanga awana zvikwereti zvishoma uye akawana zvinyorwa mumakumbo mashoma. 