The largely peaceful rallies were spearheaded by Islamist party Jamat-e-Islami (JI), but other groups including mainstream political parties joined in.
Leaders including JI chief Siraj ul Haq called for an end to the "genocide" of the Rohingya and for Pakistan to break off relations with the government in Myanmar.
Pakistan has previously expressed "deep anguish" at the violence.
Many protesters also slammed Suu Kyi, Myanmar's de facto leader, over her silence. The Nobel Peace Prize winner has faced criticism for failing to condemn the violence, leaving her global reputation in tatters.
Others have died trying to flee the fighting in Rakhine state, where witnesses say entire villages have been burned since Rohingya militants launched a series of coordinated attacks on August 25, prompting the crackdown.
In Pakistan's southern port city of Karachi, which hosts one of the largest Rohingya populations outside of Myanmar, more than 2,000 people demonstrated outside the Karachi Press Club.
In the capital Islamabad a similarly sized crowd gathered at the entrance to the diplomatic enclave, inside which the Myanmar embassy is situated.
Many carried placards reading: "Why are these Muslims being killed? What is their crime?" as chants of "Allahu Akbar", or "God is the Greatest", reverberated.
There were also some sporadic calls for "jihad", or holy war.
Security forces with protective riot gear stood nearby and containers blocked off access to the enclave, with some small scuffles.
Protests were also held in deeply religious neighbouring Afghanistan Friday.
Hundreds of placard-waving men marched in the eastern city of Jalalabad in support of the Rohingya while smaller demonstrations were held in the capital Kabul, including one outside the compound of the United Nations Assistance Mission in Afghanistan, and other cities.
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