Israel's Shin Bet internal intelligence agency is advertising jobs for speakers of the Iranian language Farsi.
Vacancies have been listed for Farsi-speaking "field co-ordinators", offering a "unique, challenging and long-term intelligence job".
Israel accuses Iran of arming Hamas and Hezbollah and has threatened to strike at its nuclear programme. Iran is a strong critic of Israel.
Israel has a sizeable Jewish population of Iranian descent.
The advertisements carried the logo and website address of the Israeli Security Agency Shabak - often referred to as the Shin Bet.
They appeared in major Israeli newspapers, including Yedioth Ahranot and Haaretz.
Candidates should have completed military service, have strong interpersonal skills and the ability to persevere, the adverts said.
In an article, Haaretz said the Shabak "apparently aims to find candidates to serve as field agents to thwart infiltration attempts by Iranian intelligence agents in Israel".
Earlier this year, a Persian Israeli was convicted of working for Iranian intelligence.
Shin Bet has said Iran tries to recruit such people when they leave to visit relatives.
The agency has followed some Western intelligence services in becoming more open about its activities in recent years, and even launched a blog last year.
It has placed recruitment ads in the press before, but has not given such specific details of the requirements in the past.
Iran is under increasing pressure from the international community over its nuclear programme.
It has recently announced plans to expand its facilities for enriching uranium, a process required to make a nuclear weapon.
Israel and the US have not ruled out a military strike against Iran's nuclear sites, although Iran's latest move is likely to be met with increased economic sanctions.
Israel also accuses Iran of arming the Lebanese militant group Hezbollah, and Hamas in Gaza, which it says has recently acquired rockets which could reach Tel Aviv.
Iran's President, Mahmoud Ahmadinejad, has called for an end to the Israeli state, and has described the Holocaust as a myth.