Kaʻahumanu's father eventually reconciled with Kamehameha I, becoming one of his closest advisors and the royal governor of Maui. He arranged for his daughter to marry the king when she was thirteen. Kamehameha had numerous wives, but Kaʻahumanu became his favorite and proved herself far more than a consort. She encouraged his campaign to unify the Hawaiian Islands under a single ruler, and when Kamehameha died on May 8, 1819, she moved swiftly. Kaʻahumanu announced that the late king had wished for her to share governance with his 22-year-old son Liholiho, who took the name Kamehameha II. The council of advisors agreed, creating the post of kuhina nui for her — a role akin to co-regent or prime minister. Her power base only grew from there, as she ruled effectively through the reigns of both Kamehameha II and Kamehameha III.

Kaʻahumanu's most radical act came not on a battlefield but at a dinner table. The ancient kapu system governed every aspect of Hawaiian life, including strict rules separating men and women during meals. Breaking a major kapu carried the death penalty. Yet Kaʻahumanu conspired with Keōpūolani, the late king's sacred wife and Kamehameha II's own mother, to eat publicly at the same table with the young king. She had already persuaded the kingdom's high priest, Hewahewa, to support abolishing the kapu entirely. When the moment came, Kamehameha II refused to execute his own mother for the violation — and with that refusal, the centuries-old system collapsed. The event, known as the ʻAi Noa, or "free eating," did not just change dining customs. It dismantled the religious framework that had structured Hawaiian society for generations.

Kaʻahumanu's methods were not always subtle. The island of Kauaʻi and its subject island Niʻihau had never been conquered by Kamehameha I. Their king, Kaumualīʻi, had become a vassal only through negotiation, not force. When Kamehameha I died, Kaʻahumanu and Kamehameha II feared Kauaʻi would break away. Their solution was blunt: on October 9, 1821, they kidnapped Kaumualīʻi and Kaʻahumanu married him by force, binding the islands together through a union the groom never chose. After Kaumualīʻi died in 1824, she married his son Kealiʻiahonui. The kingdom held together, though the means of its preservation say as much about the era's ruthless political calculus as about Kaʻahumanu's determination.

In 1824, Kaʻahumanu publicly converted to Protestant Christianity, taking the baptismal name Elizabeth. She presented Hawaiʻi with its first codified body of laws modeled on Christian ethics and the Ten Commandments. She also banned Catholic missionaries and, controversially, suppressed the practice of hula — a prohibition that would not be fully lifted until King Kalākaua's reign in 1886. In 1826, she negotiated the first treaty between Hawaiʻi and the United States under President John Quincy Adams, paying $150,000 in sandalwood to settle debts Hawaiian chiefs owed American traders. During her final illness, missionaries printed the first Hawaiian-language New Testament, bound in red leather with her name in gold letters. She kept it beside her until she died on June 5, 1832, in Mānoa Valley. Her funeral at Kawaiahaʻo Church — sometimes called the Westminster Abbey of Hawaiʻi — drew mourners from across the islands. Today her name endures on highways, shopping centers, and the Kaʻahumanu Society, a civic club founded in 1864 to honor her legacy and promote Hawaiian female leadership.