diff --git a/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.cpp b/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.cpp
index b5a87b435ff6..dd1669f29029 100644
--- a/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.cpp
+++ b/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.cpp
@@ -111,6 +111,14 @@ void RemoteInspectionTarget::unpauseForInitializedInspector()
     RemoteInspector::singleton().setupCompleted(targetIdentifier());
 }
 
+void RemoteInspectionTarget::setPresentingApplicationPID(std::optional<ProcessID>&& pid)
+{
+    m_presentingApplicationPID = pid;
+#if PLATFORM(COCOA)
+    RemoteInspector::singleton().setUsePerTargetPresentingApplicationPIDs(true);
+#endif
+}
+
 } // namespace Inspector
 
 #endif // ENABLE(REMOTE_INSPECTOR)
diff --git a/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.h b/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.h
index 7cd2abd61dcf..14098b3b7360 100644
--- a/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.h
+++ b/Source/JavaScriptCore/inspector/remote/RemoteInspectionTarget.h
@@ -29,6 +29,7 @@
 
 #include "JSRemoteInspector.h"
 #include "RemoteControllableTarget.h"
+#include <wtf/ProcessID.h>
 #include <wtf/RetainPtr.h>
 #include <wtf/TypeCasts.h>
 #include <wtf/text/WTFString.h>
@@ -62,6 +63,9 @@ class JS_EXPORT_PRIVATE RemoteInspectionTarget : public RemoteControllableTarget
     // RemoteControllableTarget overrides.
     bool remoteControlAllowed() const final;
 
+    std::optional<ProcessID> presentingApplicationPID() const { return m_presentingApplicationPID; }
+    void setPresentingApplicationPID(std::optional<ProcessID>&&);
+
 private:
     enum class Inspectable : uint8_t {
         Yes,
@@ -76,6 +80,8 @@ class JS_EXPORT_PRIVATE RemoteInspectionTarget : public RemoteControllableTarget
 #if USE(CF)
     RetainPtr<CFRunLoopRef> m_runLoop;
 #endif
+
+    std::optional<ProcessID> m_presentingApplicationPID;
 };
 
 } // namespace Inspector
diff --git a/Source/JavaScriptCore/inspector/remote/RemoteInspector.h b/Source/JavaScriptCore/inspector/remote/RemoteInspector.h
index 7a014cc45530..0a9b3787d006 100644
--- a/Source/JavaScriptCore/inspector/remote/RemoteInspector.h
+++ b/Source/JavaScriptCore/inspector/remote/RemoteInspector.h
@@ -159,6 +159,9 @@ class JS_EXPORT_PRIVATE RemoteInspector final
     void setParentProcessInformation(ProcessID, RetainPtr<CFDataRef> auditData);
     void setParentProcessInfomationIsDelayed();
     std::optional<audit_token_t> parentProcessAuditToken();
+
+    void setUsePerTargetPresentingApplicationPIDs(bool usePerTargetPresentingApplicationPIDs) { m_usePerTargetPresentingApplicationPIDs = usePerTargetPresentingApplicationPIDs; }
+
     bool isSimulatingCustomerInstall() const { return m_simulateCustomerInstall; }
 #endif
 
@@ -308,6 +311,7 @@ class JS_EXPORT_PRIVATE RemoteInspector final
     RetainPtr<CFDataRef> m_parentProcessAuditData;
     bool m_messageDataTypeChunkSupported { false };
     bool m_simulateCustomerInstall { false };
+    bool m_usePerTargetPresentingApplicationPIDs { false };
 #endif
     bool m_shouldSendParentProcessInformation { false };
     bool m_automaticInspectionEnabled WTF_GUARDED_BY_LOCK(m_mutex) { false };
diff --git a/Source/JavaScriptCore/inspector/remote/cocoa/RemoteInspectorCocoa.mm b/Source/JavaScriptCore/inspector/remote/cocoa/RemoteInspectorCocoa.mm
index 6bc571115b6c..4fa972e0edc1 100644
--- a/Source/JavaScriptCore/inspector/remote/cocoa/RemoteInspectorCocoa.mm
+++ b/Source/JavaScriptCore/inspector/remote/cocoa/RemoteInspectorCocoa.mm
@@ -453,6 +453,12 @@ static bool canAccessWebInspectorMachPort()
 
 #pragma mark - Listings
 
+static NSString* identifierForPID(ProcessID pid)
+{
+    // This format matches that used in the relay process.
+    return [NSString stringWithFormat:@"PID:%lu", (unsigned long)pid];
+}
+
 RetainPtr<NSDictionary> RemoteInspector::listingForInspectionTarget(const RemoteInspectionTarget& target) const
 {
     // Must collect target information on the WebThread, Main, or Worker thread since RemoteTargets are
@@ -493,6 +499,9 @@ static bool canAccessWebInspectorMachPort()
         break;
     }
 
+    if (auto presentingApplicationPID = target.presentingApplicationPID())
+        [listing setObject:identifierForPID(presentingApplicationPID.value()) forKey:WIRHostApplicationIdentifierKey];
+
     if (auto* connectionToTarget = m_targetConnectionMap.get(target.targetIdentifier()))
         [listing setObject:connectionToTarget->connectionIdentifier() forKey:WIRConnectionIdentifierKey];
 
@@ -722,6 +731,11 @@ static bool canAccessWebInspectorMachPort()
     if (!m_relayConnection)
         return;
 
+    // Proxy applications using per-target `presentingApplicationPID`s do not require any additional setup. The remote
+    // relay will complete its setup when the inspectable target listing is sent to it.
+    if (m_usePerTargetPresentingApplicationPIDs)
+        return;
+
     if (!m_parentProcessIdentifier || !m_parentProcessAuditData) {
         // We are a proxy application without parent process information.
         // Wait a bit for the information, but give up after a second.
diff --git a/Source/WebKit/UIProcess/WebPageProxy.cpp b/Source/WebKit/UIProcess/WebPageProxy.cpp
index 4ad63f505bda..2678c875d46f 100644
--- a/Source/WebKit/UIProcess/WebPageProxy.cpp
+++ b/Source/WebKit/UIProcess/WebPageProxy.cpp
@@ -580,6 +580,7 @@ WebPageProxy::WebPageProxy(PageClient& pageClient, WebProcessProxy& process, Ref
 
 #if ENABLE(REMOTE_INSPECTOR)
     m_inspectorDebuggable->setInspectable(JSRemoteInspectorGetInspectionEnabledByDefault());
+    m_inspectorDebuggable->setPresentingApplicationPID(m_process->processPool().configuration().presentingApplicationPID());
     m_inspectorDebuggable->init();
 #endif
     m_inspectorController->init();