The 64-year-old, whose hero is Margaret Thatcher, said that a "mountain of work" lay ahead to restore the fortunes of her ailing Liberal Democratic Party (LDP).
The LDP has governed Japan almost uninterrupted for decades but it has been haemorrhaging support as backing grows for smaller parties, including the anti-immigration Sanseito.
Takaichi, a heavy metal drummer as a student, will almost certainly be approved by parliament later this month as Japan's fifth prime minister in as many years.
She is set to face a host of complex issues including an ageing population, geopolitical upheaval, a faltering economy and growing unease about immigration.
"Together with so many of you, we have carved a new era for the LDP," Takaichi said at LDP headquarters after winning a run off vote against the telegenic and more socially progressive Shinjiro Koizumi.
"We must all pull together across all generations and work as one to rebuild (the LDP)... Everyone will have to work like a horse," she said to applause.
Koizumi, 44, would have been Japan's youngest prime minister in the modern era and represented a generational change for the LDP.
One of Takaichi's first official duties as premier will be receiving US President Donald Trump, who is reportedly set to make a stopover in Japan in late October.
Takaichi said Saturday that she had no plans to overturn Tokyo's recent trade deal -- over which questions remain -- with Washington.
Takaichi has been a strident critic of China's military build-up, and as a regular visitor to the Yasukuni war shrine her appointment may irk Beijing as well as Seoul.
Beijing's foreign ministry reacted to her win by saying "it is hoped that Japan will abide by... its political commitments on major issues such as history and Taiwan, (and) pursue a positive and rational policy toward China."
- Immigrant 'invasion' -
Primarily for LDP members, however, Takaichi's task will be to restore the fortunes of the party, which has governed almost non-stop since 1955.
Outgoing premier Shigeru Ishiba took the reins last year but his LDP-led coalition lost its majority in both houses of parliament, in part because of voter anger at inflation and an LDP slush fund scandal.
One party on the up is Sanseito, which echoes other populist movements in calling immigration a "silent invasion" and blames newcomers for a host of ills.
Japan should "reconsider policies that allow in people with completely different cultures and backgrounds", Takaichi said during the LDP campaign.
People born abroad make up just three percent of the population, and with an ageing population is in dire need of foreign workers.
"As the Japanese population is declining we need to accept foreigners, but I hope (politicians) will think about how to accept them," said Tomoyuki Mishina, 39, a real estate company employee.
- Abenomics 2.0 -
On the economy, Takaichi has in the past backed aggressive monetary easing and big fiscal spending, echoing her mentor, former premier Shinzo Abe.
Coming from the traditionalist wing of the LDP, celebrations that finally a woman is leading Japan may soon turn to disappointment.
Takaichi "has no interest in women's rights or gender equality policies," Yuki Tsuji, a professor specialising in politics and gender at Tokai University, told AFP.
Takaichi is against revising a 19th-century law obliging married couples to share the same surname, and also opposes same-sex marriage.
"An exclusive, reactionary and discriminatory political approach will persist," said Soshi Matsuoka from the LGBTQ campaign group Fair.
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