Netanyahu, who has so far failed to form a coalition after a September 17 poll, had in the past refused to give the security-oriented Bennett this coveted portfolio.
But wary of his main challenger Benny Gantz attempting to collect the support of 61 lawmakers necessary to form a coalition and become prime minister himself, the incumbent has changed course.
In doing so, he effectively locked in the three lawmakers of Bennett's New Right to his ruling Likud party.
A statement by Likud said that Netanyahu had "offered to appoint (Bennett) as defence minister, and Naftali Bennett accepted the offer."
"Bennett agreed that if a new government is formed" without a third election, "a different person will be appointed defence minister," the statement read.
The two also agreed that the New Right -- formed by Bennett and former justice minister Ayelet Shaked -- would join Likud to become a combined force, the statement said.
They will "commit to act as a joint faction throughout the current parliamentary term," it added.
Bennett did not comment on the move, but Shaked said her party had been offered a choice of the defence ministry on its own, or two portfolios for lesser ministries.
The choices available for the latter were agriculture, diaspora and welfare, Shaked said.
"In a joint decision we agreed that Bennett will be appointed defence minister until a new government is formed," she said on Twitter.
Both Likud and Gantz's Blue and White say they want a unity government, but disagree on how to achieve it.
Likud has been seeking to negotiate based on a compromise proposed by President Reuven Rivlin that takes into account the possibility Netanyahu will be indicted for corruption in the coming weeks.
It could see him remain prime minister for now, but step aside at some point later as he combats the charges.
Gantz would take over as acting premier under such a scenario.
Blue and White says Gantz should be prime minister first under any rotation arrangement since his party won the most seats, finishing with 33 compared to Likud's 32.
Whoever wants to govern needs to find partners with which to control a majority of at least 61 seats in the 120-member Israeli parliament.
Negotiators for Likud and Blue and White, as well as the heads of the two factions, have been meeting since the elections.