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Eilat is mentioned as one of the stations of the Children of Israel after The Exodus from Egypt. The original colony was probably in the northern tip of the Sea of Reeds which is now on the border with Jordan, While the later commercial port city and a center for copper corresponds to modern Aqaba, just across the border in Jordan. King David conquered Edom and took over Eilat as well.

Kings 2 14:21-22: "And all the people of Judah took Azariah, who was sixteen years old, and made him king in the room of his father Amaziah. He built Elath, and restored it to Judah, after that the king slept among his fathers."

Kings 2 16:6: "At that time Rezin king of Aram recovered Elath to Aram, and drove the Jews from Elath; and the Edomites came to Elath, and dwelt there, unto this day".

The area of Eilat was designated as part of the Jewish state in the 1947 UN Partition Plan.

During the War of Independence, the sole building in the area, an old Ottoman police station named Umm Rashrash in Arabic, was taken without a fight on March 10, 1949 as part of Operation Uvda. The Negev and Golani Brigades took part in the operation. They raised an ink-made flag ("The Ink Flag") in order to claim for Israel the area upon which Eilat would be constructed.

After the founding of Eilat some years later it became an important port as Israel's only port on the Red Sea. The Port of Eilat has high strategic and economic significance. After the 1948 Arab-Israeli War, Egypt denied passage through the Suez Canal to Israeli-flagged vessels and to non-Israeli flagged vessels carrying cargo to Israeli ports. This made Eilat crucial to Israel for access to markets in East Africa and Southeast Asia, and for the import of oil. Without recourse to Eilat, vessels sailing from Israel would have to journey through the Mediterranean and around the Cape of Good Hope to reach Southeast Asia. Such a situation took place in 1967 when Egypt's closure of the Straits of Tiran to Israeli shipping effectively closed the port of Eilat and was cited by Israel as a casus belli leading to the outbreak of the Six-Day War.