After the establishment of the State of Israel in 1948, Darwīsh witnessed massacres that forced his family to escape to Lebanon. A year later their clandestine return to their homeland put them in limbo, as they were declared “present-absent aliens.” Darwīsh left Birwa a second time in 1970 and traveled to the Soviet Union to complete his education in Moscow. He lived in Cairo, Beirut, London, and Paris, as well as Tunis, Tunisia, before returning in 1996 to live in Palestine, in the West Bank town of Ramallah. He was a member of the executive committee of the Palestine Liberation Organization (PLO) and wrote the declaration of independence issued by the Palestine National Council in 1988, but he resigned from the PLO in 1993 to protest the signing of the Oslo Accords by PLO chairman Yasīr ʿArafāt (Arafāt, Yāsirʿ). In 2000 the Israeli education minister made plans to include Darwīsh's poems of reconciliation in the school curriculum, but Israeli Prime Minister Ehud Barak (Barak, Ehud) vetoed the plan.

Darwīsh authored several books of prose and more than 20 collections of poetry. From 1981 he also served as editor of the literary journal Al-Karmel. The power of his poetry could be explained by the sincerity of his emotions and the originality of his poetic images. He borrowed from the Old and New Testaments, classical Arabic literature, Arab Islamic history, and Greek and Roman mythology to construct his metaphors. It was Darwīsh's conviction that his life in exile inspired his creative work. He often personified Palestine itself as a mother or a cruel beloved. In his single-poem volume Ḥālat ḥiṣār (2002; “A State of Siege”), Darwīsh explored the multiple reoccupations of Ramallah and described the resulting sense of Palestinian isolation. However, he foresaw a future of peace and coexistence between Israelis and Palestinians that could be achieved through dialogue between cultures. Darwīsh diverged from the political in some of his poems, relying on symbolism to relate personal experience. He devoted an entire collection, Jidāriyya (2002; “Mural”), to his brush with death following heart surgery in 1998. Collections of his poems in English translation include The Adam of Two Edens (2000), Unfortunately, It Was Paradise (2003), and The Butterfly's Burden (2007).

Darwīsh's work was translated into some two dozen languages. Among his many international awards were the Lotus Prize (1969), the Lenin Peace Prize (1983), the French medal of Knight of Arts and Belles Letters (1997), the wisām (order) of intellectual merit from Moroccan King Muhammad VI in 2000, and the 2001 Lannan Foundation Prize for Cultural Freedom. He died after undergoing heart surgery in the United States.