The announcement ended a month-long standoff after India told the ICC it would not send its team to Pakistan because of security fears and political tensions.
Under the agreement, Pakistan will also play in upcoming ICC tournaments hosted by India in other countries, yet to be decided.
"India and Pakistan matches hosted by either country at ICC Events during the 2024-2027 rights cycle will be played at a neutral venue, the ICC Board confirmed," said a statement released by the council.
"This will apply to the upcoming ICC Men's Champions Trophy 2025 (hosted by Pakistan)."
Pakistan Cricket Board (PCB) had earlier refused to play the Champions trophy on a so-called hybrid model but backed down after settling on neutral venues for both sides.
The agreement will extend to the ICC Women's Cricket World Cup 2025 hosted by India, and the ICC Men's T20 World Cup 2026 hosted by India and Sri Lanka, the statement added.
The Champions Trophy will also feature Australia, England, New Zealand, South Africa, Afghanistan and Bangladesh.
India's latest defiance is a progression of New Delhi's refusal to play bilateral cricket with Pakistan initiated after the 2008 attacks on Mumbai, which India blamed on militants based across the border.
Pakistan was also forced to host last year's Asia Cup on a hybrid model with India's matches and the final hosted in Sri Lanka.
Pakistan did, however, play in India during the 2023 ICC World Cup hosted there.
The arch-rivals only meet in ICC multi-national events like ODI and T20 World Cups, with the last bilateral series held when Pakistan toured India in 2012-13.
India last toured Pakistan to feature in the 2008 Asia Cup and have not played a bilateral series across the border for 18 years.
In the last few years, Pakistan has hosted the world's top teams after improving security, emerging from cricketing isolation that began after a militant attack on the Sri Lankan team bus in 2009 in Lahore.
