Ashigarakami District was one of the ancient subdivisions of Sagami Province, per the Nara period Ritsuryō system, under the name as . The area was under control of the later Hōjō clan in the Sengoku period, and part of Odawara Domain during the Edo period. Following disasters caused by eruptions of nearby Mount Fuji, a portion also came to be held as tenryō territory administered by the Tokugawa shogunate.