The Interior Ministry's Population and Migration Authority is to give Eritrean and Sudanese citizens who entered the country illegally the choice of leaving Israel within three months, or face being imprisoned indefinitely.
The influx largely stopped when Israel completed building a high-tech fence along its 150-mile border with Egypt in 2013. They will also be given the option of going to their home countries or third countries.
"It's baseless for Israel, a developed country, to claim that it can not take its part in carrying the burden", said Dror Sadot, spokesperson for the Hotline for Refugees and Migrants, an Israeli human rights group.
A spokesperson for Israel's Population and Immigration Authority told the BBC that there were now 38,000 "infiltrators" in Israel, of whom just 1,420 were being held in detention facilities.
Those who leave by the end of March will be given $3,500, along with airfare and other incentives. Most come from the repressive nations of Sudan and Eritrea, and are instead deported by Israel to unnamed "third countries", known to be Rwanda and Uganda.
"The Israeli government's decision to expel 40,000 African asylum seekers is of great concern", he said.
On another note, the jewish state exempts elderly people, children and people who suffered slavery and trafficking from this ultimatum.
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"Today the Cabinet will approve the plan for deporting the infiltrators from Israel", said Prime Minister Benjamin Netanyahu in a statement.
"We have expelled about 20,000 and now the mission is to get the rest out", Netanyahu said.
According to Israeli authorities these people are seeking economic opportunities and not asylum therefore their claim to be refugees is void.
According to Israel's program, migrants have until the end of March to leave, each will receive a plane ticket and 2,900 euros to do so, and those who remain in Israeli territory will be arrested.
However, the High Court also ruled that since the deportations may only be carried out with the agreement of the migrants, refusal to leave Israel can not be considered uncooperative behavior.
The Center for Refugees and Migrants, Amnesty International Israel, the Association for Civil Rights in Israel and other groups signed a letter calling for the expulsions to be stopped.
Since 2009 when Israel took over the process from the UNHCR to determine who is a refugee, only eight Eritreans and two Sudanese have been granted this status.