Cunningham began her photographic career in Seattle, Washington, acquiring her first camera from a mail-order correspondence school around 1905. In 1907 she worked in Edward S. Curtis’s studio where she learned to re-touch negatives and to make platinum prints and in 1909 she went to Dresden where she studied photochemistry. The following year she met Alfred Stieglitz and Gertrude Käsebier after which she set up her own studio in Seattle. Beginning as a pictorialist, she was involved with the Pictorial Photographers of America until her relocation to California in 1921 when her work became more modern.

Cunningham married the etcher Roi Partridge (there are two prints by him in the Johnson’s collection) and moved to California where she met Edward Weston. In 1932 Cunningham joined the group of West Coast photographers, founded by Ansel Adams and Willard Van Dyke in 1934 under the name of Group f.64. They met to talk about photography and to show their prints to each other and to the public. After the breakup of Group f.64, Cunningham ran a portrait gallery and taught at the San Francisco Art Institute.