An Israeli air strike destroyed a car in Gaza City on Monday night, killing commander Majed al-Harazeen and another fighter, the Islamic Jihad said.
"The assassination of the general commander will open the door wide to a wave of martyrdom operations," the group's al-Quds Brigades armed wing said.
The car had been full of explosives and a huge explosion could be heard across the city.
Hundreds of Islamic Jihad fighters gathered in the streets and fired into the air after the attack.
Hours later, a second Israeli attack killed three other Islamic Jihad fighters, including the rocket maker, on the streets of Gaza City, the group said.
An Israeli army spokeswoman said the attacks targeted fighters preparing to fire rockets at Israel.
Medical workers said the attacks also wounded two bystanders.
Islamic Jihad claims responsibility for most of the rocket attacks from Gaza against Israel and Israel accused al-Harazeen of being one of the key leaders behind those attacks.
Palestinian officials said al-Harazeen, who had been on Israel's most wanted list for nine years, was the most senior commander to be killed in an Israeli strike in the Hamas-controlled Gaza Strip in more than a year.