The Liberal Democratic Party, which has ruled Japan for almost all of the postwar era, elected Takaichi, 64, on Saturday to regain trust from a public angered by rising prices and drawn to opposition groups promising stimulus and clampdowns on migrants.
A vote in parliament to choose a replacement for outgoing Shigeru Ishiba is expected on October 15.
Takaichi is favoured as the ruling coalition has the largest number of seats.
Takaichi, the only woman among the five LDP candidates, prevailed in a run-off against the more moderate Shinjiro Koizumi, 44, who was bidding to become Japan's youngest modern leader.
A former economic security and internal affairs minister with an expansionary fiscal agenda for the world's fourth-largest economy, Takaichi takes over a party in crisis.
Other parties, including the expansionist Democratic Party for the People and the anti-immigration Sanseito, have been steadily luring voters, especially younger ones, away from the LDP.
The LDP and its coalition partner lost their majorities in both houses under Ishiba in the past year, triggering his resignation.
"Recently, I have heard harsh voices from across the country saying we don't know what the LDP stands for any more," Takaichi said in a speech before the run-off vote.
"That sense of urgency drove me. I wanted to turn people's anxieties about their daily lives and the future into hope."
Takaichi, who says her hero is Margaret Thatcher, Britain's first female prime minister, offers a starker vision for change than Koizumi and is potentially more disruptive.
An advocate of late premier Shinzo Abe's "Abenomics" strategy to boost the economy with aggressive spending and easy monetary policy, she has previously criticised the Bank of Japan's interest rate increases.
Such a spending shift could spook investors worried about one of the world's biggest debt loads.
At a media conference, Takaichi laid out various plans to cut taxes and increase subsidies but said she understood "the importance of fiscal prudence".
Takaichi said she planned to honour an investment deal with US President Donald Trump that lowered his punishing tariffs in return for Japanese taxpayer-backed investment, having previously mooted the possibility of redoing it.
The US ambassador to Japan, George Glass, congratulated Takaichi, posting on X that he looked forward to strengthening the Japan-US partnership "on every front".
But her nationalistic positions - such as her regular visits to the Yasukuni shrine to Japan's war dead, viewed by some Asian countries as a symbol of its past militarism - might rile neighbours such as South Korea and China.
South Korea would seek to "co-operate to maintain the positive momentum in South Korea-Japan relations", President Lee Jae-myung's office said in a statement.
Takaichi also favours revising Japan's pacifist postwar constitution and suggested in 2025 that Japan could form a "quasi-security alliance" with Taiwan, the democratically governed island claimed by China.
Taiwan President Lai Ching-te welcomed her election, saying she was a "steadfast friend of Taiwan".
If elected prime minister, Takaichi said she would travel overseas more regularly than her predecessor to spread the word that "Japan is Back!"
Some of her supporters viewed her selection as a watershed in Japan's male-dominated politics.
However, her socially conservative positions - such as opposing changes to allowing married couples to have separate surnames - make her more popular among men than women, opinion polls show.
Her conservative appeal, however, might help blunt the rise of Sanseito.
Echoing Sanseito's warnings about foreigners, she promised to clamp down on rule-breaking visitors and immigrants, who have come to Japan in record numbers in recent years.
