Kerry's meetings were meant to assure his counterparts from the six-member Gulf Cooperation Council, a group of critical allies disappointed by what they see as a continued deterioration of their relationship with the United States amid Iran's changing role in the region.
The United States wants to see the Gulf countries do more to take on ISIS, which it views as the paramount concern in the region.
But the Gulf states see Iran as the biggest regional threat, driving their stances on conflicts ranging from Syria to Yemen, and have expressed frustration that the United States hasn't done more to counter Iran since a landmark nuclear deal eased tensions between the two sworn enemies.
Since the outlines of that deal were struck a year ago, Iran has engaged in ballistic missile tests, deepened its involvement in Syria and increased weapons shipments to Houthi rebels in Yemen.
Gulf states: Iran is 'dangerous as ever'
Standing next to Kerry, Bahraini Foreign Minister Khalid bin Ahmed al Khalifa said Iran's "hegemonic interventions" are "continuing unabated."
And in an op-ed published this week in The Wall Street Journal, the United Arab Emirates' ambassador to the United States, Yousef Al Otaiba, said Iran "is as dangerous as ever."
Following Thursday's talks, Saudi Foreign Minister Adel al-Jubeir said Gulf Arab states rejected the intervention of Iran into their internal affairs and what he called its attempts to smuggle weapons into some GCC states.
"If Iran continues its aggressive policies and continues to intervene into the affairs of the GCC states, it will be difficult to deal with Iran," he said.
The differing approaches between the Gulf states and the United States on a path forward for Syria illustrates the disconnect between the allies over Iran.
A fragile ceasefire put in place February between regime forces and opposition fighters has largely held, but recent flare-ups have stalled talks on a political solution to end the Syrian conflict.
Kerry urged Gulf states to use their influence with Syrian opposition leaders, saying after the talks, "We will need to apply all of our efforts in order to maintain not only the cessation of hostilities but to build some possible momentum in the negotiations themselves."
The United States is fixated on defeating ISIS, which it sees as the most strategic threat. Washington's public line is that Syrian President Bashar al-Assad has to go but has left the time line of his departure vague.
Gulf nations, led by Saudi Arabia, often say a lack of U.S. leadership to help end the Syrian civil war created the conditions for ISIS' rise from the chaos in that country.
They are focused on the departure of Assad, who is closely supported by Iran. They see allies and proxies of Iran, from Assad to Hezbollah to other Shiite militias in the region, as a bigger strategic regional threat than the Sunni ISIS.
Kerry: We want a 'peaceful solution'
Kerry said following the talks that the United States was "prepared to find a peaceful solution to these issues, and we look for Iran to make it clear to everybody that they are prepared to cease these kinds of activities that raise questions about credibility and questions about intention."
"If Iran wants to be part of a constructive resolution to Syria, a constructive resolution to Yemen, it can be so," Kerry added. "But it is not constructive to be sending dhows across the Gulf loaded with weapons that are only going to add fuel to the fire of a war we are busy trying to end."
Last week, the U.S. Fifth Fleet seized an Iranian shipment of AK-47s and rocket-propelled grenade launchers that Kerry said was "clearly moving in the direction of Yemen."
The United States generally views the Saudi-led intervention in Yemen, whose government is under attack from Iran-backed rebels, as a diversion of Gulf resources and political attention from the fight against ISIS.
Washington initially endorsed the campaign against Houthi rebels. But Gulf officials have been frustrated that they haven't received more support from the United States in their battle to restore Abdu Rabu Mansour Hadi to power.
U.S. officials privately grumble that the fighting has allowed al Qaeda in the Arabian Peninsula -- al Qaeda's most deadly branch in the region -- and ISIS to strengthen their gains in Yemen.
Coupled with continued U.S. pressure to end the intervention, the Gulf sees it as yet another data point illustrating how the United States doesn't understand the threat Iran and its proxies and allies pose to them, even as they have supported American operations in their region for years.
In an interview with The Atlantic magazine last month. Obama decried U.S. allies in the Persian Gulf as sometimes being "free riders" eager to drag the United States into open-ended sectarian conflicts that sometimes did not dovetail with American interests.
Griping that the competition between Saudi Arabia and Iran was helping to feed proxy wars in Syria, Iraq and Yemen, Obama said the two rivals "need to find an effective way to share the neighborhood and institute some sort of cold peace."
A shift in relations with Iran
Experts said the remarks signaled a shift away from America's long-standing policy of containing Iran toward one of rapprochement.
"For them, it was kind of like suggesting America shares their region with al Qaeda. It hit that hard and personally and showed the President doesn't fully understand the concern they have with Iran's activities and the impact it has on their own states," " said Lori Plotkin Boghardt, a fellow at the Washington Institute for Near East Policy who specializes in Arab Gulf politics and U.S.-Gulf relations.
Thursday's talks followed on a set of commitments made last year at Camp David, where Obama held a summit of Gulf leaders as the nuclear deal with Iran curbing Tehran's nuclear program in exchange for sanctions relief was being worked out.
To reassure U.S. allies uneasy about the deal, the President pledged additional military aid and offered to help boost regional defense efforts on missile defense, cybersecurity and terrorism.
The United States has expedited the sale and delivery of military equipment, but officials said more work remains on how a regional missile defense could be deployed.
Earlier in the day, Kerry visited the naval base that hosts the U.S. Fifth Fleet, where U.S. Navy ships are taking part in a monthlong multinational exercise to keep vital sea lanes open.
"You maintain a presence that sends a message to any country that wants to mess around that we mean business," he told American servicemen.