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The season opens with Coulson's team abducted from a diner and thrown through a monolith to an unknown place. Only Fitz is left behind. The others wake up on the Lighthouse, a space station where the last humans live enslaved by the Kree under the cruel Kasius. Earth outside is in pieces. They learn they're more than 70 years in the future and that the planet's destruction is blamed on Daisy, Quake.
On the Lighthouse the team meets Deke Shaw, a clever, selfish survivor who ends up an ally. Yo-Yo finds a clue about her own future and starts to fear what's coming. Fitz, back in the present, gets help from Lance Hunter, figures out how to reach his friends and goes into cryo for 74 years to wake up in the future. The couple reunites, Kasius falls and the group finds a way to rebuild the monolith and go home.
Back in the present, nothing is settled. S.H.I.E.L.D. is hunted as a fugitive agency, and General Hale, tied to Hydra, wants to create a "destroyer of worlds" using gravitonium and her own daughter, Ruby. Soon after, Ruby cuts off both of Yo-Yo's arms. Fitz and Simmons get married in the show's 100th episode. Right after comes the bad news: Coulson is dying. His deal with Ghost Rider burned away whatever was keeping him alive. Fitz also shows a dark, dangerous side, a leftover from a virtual reality in his past.
The final villain is General Glenn Talbot. Manipulated by Hydra and convinced he must defend Earth from Thanos, he absorbs gravitonium and becomes Graviton. The team tries everything to avoid the future they saw. In the decisive battle in Chicago, Daisy uses a serum and blasts Talbot into space. The timeline changes, but the cost is high: Fitz dies under the rubble in Simmons's arms.
Coulson refuses the treatment that could save him and goes to spend his last days in Tahiti with May. Daisy takes the lead. The season closes on a hope: the Fitz who died was the one who traveled to the future. This timeline's Fitz is still frozen in space aboard Enoch's ship. Simmons sets off to find him.