Oliver spent his early career as a teacher at the Ashland school as well as a member of the Mountain Rangers. He quickly rose through the ranks starting as a private and moved to captain in 3 years. 

In 1865, Oliver was appointed assistant to the United States Indian Agent, who also happened to be his father. From there, Oliver spent several years working under multiple agency administrations which allowed him to gain influence over the tribes of southeastern Oregon. The influence he gained would proved to be beneficial when the Modoc outbreak in 1872 happened. This led to the conversion of the most resistant Indian Tribes to farmers and stockmen.

In 1876, friends of Oliver Applegate wanted him to use his experience, from working with Indian affairs, to be appointed general Indian Agent for Oregon. In 1989, Applegate became the United States Indian Agent of the Klamath Reservation until Congress discontinued the position 5 years later.

In 1878, Applegate started a position as Editor of the Ashland Tidings and married Miss Ella Anderson. Oliver Applegate had 6 kids between 1879 and 1896.