Cullen began writing and publishing poetry in the early 1920s while still a college undergraduate, and published widely in both African American oriented magazines and mainstream venues like Poetry. His first published book of poetry, Color, was published in the fall of 1925, and contains several landmark poems, including "Heritage," Incident," and "Yet Do I Marvel." The collection was very well-received by both the African American and mainstream white press. The illustrations in later editions of this book, and in other books of poetry by Countee Cullen published in the 1920s, were by Charles Cullen, a white graphic artist of no relation to Countee Cullen.
Notably, in 1925 Cullen also won two important literary prizes sponsored by African American magazines. In May 1925, Cullen was awarded second prize for Opportunity's poetry contest (for "For One Who Said Me Nay"). Later, Cullen would join the editorial staff of Opportunity, and publish a regular column there on arts and literature (1925-1927). In October 1925, Cullen also won first prize in the Spingarn Prize competition sponsored by The Crisis. As part of that contest, two of Cullen's poems were printed in the October, 1925 issue of the magazine along with a photograph of the young poet.
After Color, Cullen soon published The Ballad of the Brown Girl (1927), Copper Sun (1927), and The Black Christ (1929); these works are presently still in copyright. He also received a Guggenheim Fellowship in 1928, which allowed him to travel back and forth between France and the U.S. between 1928 and 1934. (In this respect his career bears some similarities to writers like Claude McKay and Langston Hughes, who also traveled extensively in Europe early in their careers.) Cullen also published an important anthology of poetry by Black writers in 1927, Caroling Dusk: an Anthology of Verse by Black Poets of the Twenties, which contained poems by a large range of emerging writers, some of whom were too young to have appeared in earlier Harlem Renaissance anthologies.
Cullen is thought to have been gay, though he was married to women twice and the documentation of his relationships with men is somewhat sketchy. Cullen married Yolande Du Bois, daughter of the noted scholar and author W.E.B. Du Bois, in 1928, but the marriage was unsuccessful and the two were divorced in 1930. Later, Cullen married Ida Roberson.