Sam Rainsy, head of the Cambodia National Rescue Party (CNRP), is seen as the main challenger to strongman Prime Minister Hun Sen, who has ruled Cambodia for nearly three decades.
A deal between the two rivals on Tuesday saw the CNRP end a boycott of parliament triggered by last July's disputed election.
The opposition accused Hun Sen's Cambodian People's Party of stealing the election by rigging ballots.
Rainsy was removed from the electoral register months before that election because of criminal convictions that were later pardoned.
Analysts said his removal reflected Hun Sen's concern at the opposition's rising popularity.
Rainsy will replace a CNRP lawmaker who has stood down, a party spokesman told AFP, adding the party would finalise his application to become a lawmaker by the end of Thursday.
The National Election Committee (NEC) said the switch was legal as Rainsy had been re-registered on the voter list, and the party's reserve candidates in the constituency where the CNRP lawmaker had stepped down had all resigned.
"The main condition is that he has to be on the voter list, and he has already registered on the voter list. So there is no problem for him," secretary general of the NEC Tep Nytha said.
Until a surprise royal pardon just before the election, Rainsy had faced 11 years in jail if he returned to Cambodia for convictions -- in absentia -- of crimes he contends were politically motivated.
The pardon came too late for him to run for parliament.
After talks between Hun Sen and Rainsy on Tuesday, the CNRP agreed to end its boycott and take up its seats in the National Assembly in return for a promise of electoral reforms.
Their swearing-in ceremony could take place over coming days.
Hun Sen, 61, is regularly criticised by campaigners for ignoring human rights and stamping out dissent.
Despite securing victory at the disputed poll, the CPP lost 22 seats in a sign of falling support for the strongman -- a former Khmer Rouge cadre who has vowed to remain in power until he is 74.