The fate of occupied Jerusalem is on the summit's agenda, as the United States prepares to move its embassy from Tel Aviv to the disputed city after declaring it the capital of Israel.
Saudi Arabia slammed longtime rival Iran on Sunday following western missile strikes on Syria, an ally of Tehran, last week.
"The summit condemned Iranian interference in the internal affairs of Arab countries, either through igniting sectarian strife or planting militias in Arab countries such as Lebanon, Iraq and Yemen, and harboring al Qaeda terrorists", Saudi Foreign Minister Adel Jubeir told a news conference.
Iran also openly supports the Shia Houthi rebels in Yemen in their war against the Saudi-backed government but denies accusations of smuggling arms to the insurgents.
"We extend our support to the Palestinians' right to establish their homeland based on the 1967 lines with the capital city Jerusalem, as stated in the global resolutions and Arab peace initiative", said Al-Jubeir during his speech at foreign ministers' preparatory meeting on Friday.
"The league's final statement was clearly under the heavy shadow of Saudi Arabia's destructive policies", he added.
The Arab leaders participating in the summit have affirmed centrality of the Palestinian issue and importance of the status of eastern Jerusalem as the capital of the future state of Palestine.
The summit will offer an opportunity for Arab leaders to hold smaller meetings on the sidelines to discuss and coordinate on a wide range of issues, including how to move forward on Syria, how to handle the tense situation in Gaza, and what to do about Libya.
Saudi Arabia pushed for a tough, unified stance against Iran at the annual gathering of the 22-member Arab League.
The King welcomed the statement issued by the Security Council, which strongly condemned the launching of Iran-made ballistic missiles by the Houthi militia on Saudi cities.
The summit also comes with Saudi Arabia and Qatar locked in a monthslong diplomatic standoff, with Riyadh accusing Doha of supporting extremists and being too close to Iran.
In attendance were leaders from the Middle East and North Africa, including Egyptian President Abdel Fattah al-Sisi and Jordanian King Abdullah.
The Arab League was founded in 1945 to protect newly-won independence throughout the region.
Western states have accused the forces of Syrian President Bashar al-Assad of an April 7 attack using chemicals in the Syrian town of Douma.