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Foreign minister (1956–1966)

In October 1955, Ben-Gurion appointed Meir as foreign minister, replacing Sharett. The occasional disagreements between Ben-Gurion and Sharett had escalated to snubbing in meetings and refusals to speak face-to-face. Meir, while less experienced in foreign affairs than Sharett, had a consistently loyal and friendly relationship with Ben-Gurion. While Meir eventually came to enjoy her new job, she disliked the lingering pro-Sharett colleagues in her department.

Meir served as foreign minister from 18 June 1956 to 12 January 1966. Her first months as Foreign Minister coincided with the 1956 Suez Crisis, in which Israel, Britain, and France invaded Egypt to regain Western control over the Suez Canal, remove the President of Egypt Gamal Abdel Nasser, and secure freedom of navigation through the Straits of Tiran for Israel. Meir planned and coordinated with the French government and military prior to the start of the invasion. During United Nations debates about the crisis, Meir took charge of the Israeli delegation. After the fighting started, the United States, the Soviet Union, and the United Nations forced the three invaders to withdraw.

As foreign minister, Meir promoted ties with the newly established states in Africa in an effort to gain allies in the international community. She also believed that Israel had experience in nation-building that could be a model for the Africans. In her autobiography, she wrote:

Like them, we had shaken off foreign rule; like them, we had to learn for ourselves how to reclaim the land, how to increase the yields of our crops, how to irrigate, how to raise poultry, how to live together, and how to defend ourselves. Israel could be a role model because it had been forced to find solutions to the kinds of problems that large, wealthy, powerful states had never encountered.

She also devoted much effort to convincing the United States to sell Israel weaponry. One success in this area came in 1962, when the White House quietly agreed to sell Hawk missiles to Israel. Israel's relationship with the Soviet Union remained frosty during her tenure.

On 29 October 1957, Meir's foot was slightly injured when a Mills bomb was thrown into the debating chamber of the Knesset. David Ben-Gurion and Moshe Carmel were more seriously injured. The attack was carried out by 25-year-old Moshe Dwek. Born in Aleppo, his motives were attributed to a dispute with the Jewish Agency, but he was described as being "mentally unbalanced".

In 1958, shortly after the death of Pope Pius XII, Meir praised the late pope for assisting the Jewish people. The pontiff's legacy as a wartime pope has continued to be controversial into the 21st century.

The same year, during the wave of Jewish migration from Poland to Israel, Meir sought to prevent disabled and sick Polish Jews from immigrating to Israel. In a letter sent to Israel's ambassador in Warsaw, Katriel Katz, she wrote:

A proposal was raised in the coordination committee to inform the Polish government that we want to institute selection in aliyah, because we cannot continue accepting sick and handicapped people. Please give your opinion as to whether this can be explained to the Poles without hurting immigration."

In late 1965, 67-year-old Meir was diagnosed with lymphoma. In January 1966, she retired from her role as Foreign Minister, citing exhaustion and ill health, although she continued to serve in the Knesset and as secretary-general of Mapai.

During the 1960s, Meir lived in a flat on the upper level of a house that was once known as Villa Harun al-Rashid. The house was built in 1926 by Hanna Bisharat and later rented to British officers. The house was later given to Zionist militias, due to the prominent view from the roof. According to Hanna Bisharat's grandson George Bisharat, Meir had the tiles on the house's front sandblasted "to obliterate the 'Villa Harun ar-Rashid' and thereby conceal the fact that she was living in an Arab home."