Following an eight-year hiatus from feature filmmaking, Jenkins directed and co-wrote the LGBTQ-themed independent drama Moonlight (2016), which won numerous accolades, including the Academy Award for Best Picture.

Jenkins received an Oscar nomination for Best Director and jointly won the Academy Award for Best Adapted Screenplay with Tarell Alvin McCraney.

He released his third directorial feature If Beale Street Could Talk in 2018 to critical praise, and earned nominations for his screenplay at the Academy Awards and Golden Globes.

[4][10] As a teenager Jenkins lived with friends from Miami Northwestern Senior High School, at which he played football and ran track.

[6] Jenkins studied film at the Florida State University College of Motion Picture Arts (FSU),[3] where he met many of his future frequent collaborators, including cinematographer James Laxton, producer Adele Romanski and editors Nat Sanders and Joi McMillon.

To resolve his personal misgivings, in a divergence from the inspirations of his classmates, he looked toward foreign arthouse cinema and directors like Wong Kar-wai, Claire Denis, Hou Hsiao-hsien, and Lynne Ramsay.

Four days after graduating from FSU, he moved to Los Angeles to pursue a filmmaking career, spending two years working on various projects as a production assistant.

[11] Previously he had fretted over his chances of success due to his racial and class identity, but My Josephine demonstrated that "I could do the work to make myself as accomplished as anyone else".

[17][18] The impetus being the lack of low-budget mumblecore films which featured African-Americans, Jenkins recalled that the movie represented the "place where I was both physically, emotionally, and mentally".

[13][19] Well received by critics, the film underwent "the usual tour of festivals garnering its share of nominations, reviews, small awards and limited release distribution in major cities in 2009 and 2010".

[4][20] Following Medicine for Melancholy, Jenkins wrote multiple scripts: a time travel epic for Focus Features and adaptations of If Beale Street Could Talk and a memoir by Bill Clegg.

[31][32][33] Anthropologist Elizabeth Davis stated that Moonlight and similar films' acclaim indicates an "increase in the social and institutional recognition and approval of blackness".

[34] In 2022, in a poll of 1,639 participating critics, programmers, curators, archivists and academics, Sight and Sound crowned Moonlight as the 60th greatest film of all time.

[35] In 2017, Jenkins directed the fifth episode of the Netflix original series Dear White People, having been chosen due to his work on Moonlight.

The main cast of The Underground Railroad includes Thuso Mbedu as Cora, with Chase W. Dillon as Homer and Aaron Pierre as Caesar.

[42][43] "[Bringing] together a group of disparate artists", Jenkins and the casting director, Francine Maisler, searched worldwide for an actor to play Cora and sought those then-undiscovered.

[60] He credits his romantic partner and fellow filmmaker Lulu Wang with inspiring him, "add[ing] rigor to creative practice".

[11] Morgan Jerkins opined that Jenkins, who re-reads texts he's adapting, "is not only a filmmaker but also a bibliophile who pulls from both historical and contemporary sources".

[10] Despite a more intense plot and themes, discussing parenting, friendship, and black masculinity, especially in regards to sexual orientation, Jenkins made the decision to invert Medicine for Melancholy's sombre color palette in Moonlight; he wished for the audience to be immersed and for there to be a "softness around the characters" – a desire also reflected in his choice of aspect ratio, 2:35.

[13][61] Moonlight, If Beale Street Could Talk and The Underground Railroad compose, in the eyes of Jenkins, a thematic trilogy, exploring childhood abandonment – including his own feelings.

[46] Adele Romanski identified Medicine for Melancholy, Moonlight, If Beale Street Could Talk as variations upon a template: a love story.

[33] Jenkins has stated that, amidst his solemn consideration of the craft and formalism of film, he seeks to articulate his "personal experience, what it feels like to be a young black man in America" – his perception evident in My Josephine, and surmised to be in Moonlight, saying of the former "it fucking worked.

[5] After The Underground Railroad's release Felix wrote that Jenkins "is breaking the fourth wall to help Black people look themselves in the eye".