diff --git a/internal/flow/processor/content.go b/internal/flow/processor/content.go
index d8a83eb4d..1369e2ef8 100644
--- a/internal/flow/processor/content.go
+++ b/internal/flow/processor/content.go
@@ -183,6 +183,10 @@ func (p *ContentRequestProcessor) ProcessRequest(
 			}
 		}
 		messages = p.getIncrementMessages(invocation, summaryUpdatedAt)
+		// When summary is present, ensure messages start with user role to comply with API requirements.
+		if !summaryUpdatedAt.IsZero() {
+			messages = p.trimLeadingNonUserMessages(messages)
+		}
 		req.Messages = append(req.Messages, messages...)
 		needToAddInvocationMessage = summaryUpdatedAt.IsZero() && len(messages) == 0
 	}
@@ -328,13 +332,33 @@ func (p *ContentRequestProcessor) mergeUserMessages(
 	return merged
 }
 
+// trimLeadingNonUserMessages removes leading non-user messages from the slice.
+// This ensures that when summary is present, the incremental messages start with
+// a user message to comply with API requirements (system messages must be followed by user).
+//
+// Note: Under normal operation, summary is only triggered after final assistant responses
+// (not user messages, tool calls, or tool results), so the incremental messages should
+// already start with a user message. This function serves as a defensive measure for
+// edge cases or potential future changes.
+func (p *ContentRequestProcessor) trimLeadingNonUserMessages(messages []model.Message) []model.Message {
+	for i, msg := range messages {
+		if msg.Role == model.RoleUser {
+			return messages[i:]
+		}
+	}
+	// No user message found, return empty slice.
+	return nil
+}
+
 func (p *ContentRequestProcessor) shouldIncludeEvent(evt event.Event, inv *agent.Invocation, filter string,
 	isZeroTime bool, since time.Time) bool {
 	if evt.Response == nil || evt.IsPartial || !evt.IsValidContent() {
 		return false
 	}
 
-	if !isZeroTime && evt.Timestamp.Before(since) {
+	// Use !After instead of Before to exclude events at exactly the summary boundary.
+	// This prevents the last summarized event from appearing in both the summary and incremental messages.
+	if !isZeroTime && !evt.Timestamp.After(since) {
 		return false
 	}
 
diff --git a/runner/runner.go b/runner/runner.go
index 27afdd43a..0d19da37a 100644
--- a/runner/runner.go
+++ b/runner/runner.go
@@ -316,7 +316,13 @@ func (r *runner) handleEventPersistence(
 		return
 	}
 
-	// Trigger summarization immediately after appending a qualifying event.
+	// Trigger summarization only after final assistant responses.
+	// Skip user messages, tool calls, and tool results to ensure summary
+	// always contains complete Q&A pairs (including tool call round-trips).
+	if agentEvent.IsUserMessage() || agentEvent.IsToolCallResponse() || agentEvent.IsToolResultResponse() {
+		return
+	}
+
 	// Use EnqueueSummaryJob for true asynchronous processing.
 	// Prefer filter-specific summarization to avoid scanning all filters.
 	if err := r.sessionService.EnqueueSummaryJob(