diff --git a/vaadin-combo-box-flow-parent/vaadin-combo-box-flow-integration-tests/src/main/java/com/vaadin/flow/component/combobox/test/MultiSelectComboBoxThrottledProvider.java b/vaadin-combo-box-flow-parent/vaadin-combo-box-flow-integration-tests/src/main/java/com/vaadin/flow/component/combobox/test/MultiSelectComboBoxThrottledProvider.java
new file mode 100644
index 00000000000..8e67d4cd7c5
--- /dev/null
+++ b/vaadin-combo-box-flow-parent/vaadin-combo-box-flow-integration-tests/src/main/java/com/vaadin/flow/component/combobox/test/MultiSelectComboBoxThrottledProvider.java
@@ -0,0 +1,45 @@
+/*
+ * Copyright 2000-2025 Vaadin Ltd.
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License"); you may not
+ * use this file except in compliance with the License. You may obtain a copy of
+ * the License at
+ *
+ * http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS, WITHOUT
+ * WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied. See the
+ * License for the specific language governing permissions and limitations under
+ * the License.
+ */
+package com.vaadin.flow.component.combobox.test;
+
+import java.util.stream.IntStream;
+
+import com.vaadin.flow.component.combobox.MultiSelectComboBox;
+import com.vaadin.flow.component.html.Div;
+import com.vaadin.flow.data.provider.DataProvider;
+import com.vaadin.flow.router.Route;
+
+@Route("multi-select-combo-box-throttled-provider")
+public class MultiSelectComboBoxThrottledProvider extends Div {
+
+    public MultiSelectComboBoxThrottledProvider() {
+        setSizeFull();
+        var comboBox = new MultiSelectComboBox<String>();
+        comboBox.setItems(DataProvider.fromFilteringCallbacks(query -> {
+            int offset = query.getOffset();
+            int limit = query.getLimit();
+            int end = Math.min(offset + limit, 1000);
+            try {
+                Thread.sleep(500);
+            } catch (InterruptedException e) {
+                throw new RuntimeException(e);
+            }
+            return IntStream.range(offset, end)
+                    .mapToObj(i -> "Item " + (i + 1));
+        }, query -> 1000));
+        add(comboBox);
+    }
+}
diff --git a/vaadin-combo-box-flow-parent/vaadin-combo-box-flow-integration-tests/src/test/java/com/vaadin/flow/component/combobox/test/MultiSelectComboBoxThrottledProviderIT.java b/vaadin-combo-box-flow-parent/vaadin-combo-box-flow-integration-tests/src/test/java/com/vaadin/flow/component/combobox/test/MultiSelectComboBoxThrottledProviderIT.java
new file mode 100644
index 00000000000..77f3af4f1f6
--- /dev/null
+++ b/vaadin-combo-box-flow-parent/vaadin-combo-box-flow-integration-tests/src/test/java/com/vaadin/flow/component/combobox/test/MultiSelectComboBoxThrottledProviderIT.java
@@ -0,0 +1,53 @@
+/*
+ * Copyright 2000-2025 Vaadin Ltd.
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License"); you may not
+ * use this file except in compliance with the License. You may obtain a copy of
+ * the License at
+ *
+ * http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS, WITHOUT
+ * WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied. See the
+ * License for the specific language governing permissions and limitations under
+ * the License.
+ */
+package com.vaadin.flow.component.combobox.test;
+
+import org.junit.Assert;
+import org.junit.Before;
+import org.junit.Test;
+import org.openqa.selenium.Keys;
+
+import com.vaadin.flow.component.combobox.testbench.MultiSelectComboBoxElement;
+import com.vaadin.flow.testutil.TestPath;
+import com.vaadin.tests.AbstractComponentIT;
+
+@TestPath("multi-select-combo-box-throttled-provider")
+public class MultiSelectComboBoxThrottledProviderIT
+        extends AbstractComponentIT {
+    private MultiSelectComboBoxElement comboBox;
+
+    @Before
+    public void init() {
+        open();
+        comboBox = $(MultiSelectComboBoxElement.class).waitForFirst();
+    }
+
+    @Test
+    public void selectItem_blurWhileLoading_reopen_itemsCorrectlyLoaded() {
+        comboBox.openPopup();
+        comboBox.waitForLoadingFinished();
+        // Add a filter
+        comboBox.sendKeys("Item");
+        comboBox.waitForLoadingFinished();
+        // Choose the first item
+        comboBox.sendKeys(Keys.DOWN, Keys.ENTER, Keys.TAB);
+        Assert.assertTrue(comboBox.getSelectedTexts().contains("Item 1"));
+
+        comboBox.openPopup();
+        comboBox.waitForLoadingFinished();
+        Assert.assertFalse(comboBox.getOptions().isEmpty());
+    }
+}
diff --git a/vaadin-combo-box-flow-parent/vaadin-combo-box-flow/src/main/java/com/vaadin/flow/component/combobox/ComboBoxDataController.java b/vaadin-combo-box-flow-parent/vaadin-combo-box-flow/src/main/java/com/vaadin/flow/component/combobox/ComboBoxDataController.java
index a432d40e1ec..454f1e6afed 100644
--- a/vaadin-combo-box-flow-parent/vaadin-combo-box-flow/src/main/java/com/vaadin/flow/component/combobox/ComboBoxDataController.java
+++ b/vaadin-combo-box-flow-parent/vaadin-combo-box-flow/src/main/java/com/vaadin/flow/component/combobox/ComboBoxDataController.java
@@ -145,6 +145,8 @@ public void initialize() {
     // provided.
     private String lastFilter;
 
+    private boolean needsForceResetOnReopen = false;
+
     private SerializableConsumer<String> filterSlot = filter -> {
         // Just ignore when setDataProvider has not been called
     };
@@ -280,8 +282,12 @@ void setViewportRange(int start, int length, String filter) {
         // results in it not sending an update. However, the client needs to
         // receive an update in order to clear the loading state from opening
         // the combo box.
-        if (lastFilter == null) {
+        if (lastFilter == null
+                || comboBox.isOpened() && needsForceResetOnReopen) {
             dataCommunicator.reset();
+            if (comboBox.isOpened()) {
+                needsForceResetOnReopen = false;
+            }
         }
         dataCommunicator.setViewportRange(start, length);
         filterSlot.accept(filter);
@@ -587,7 +593,13 @@ private void setClientSideFilter(boolean clientSideFilter) {
     private void clearFilterOnClose(PropertyChangeEvent event) {
         if (Boolean.FALSE.equals(event.getValue())) {
             if (lastFilter != null && !lastFilter.isEmpty()) {
+                // Clear non-empty filter and set flag to force reset on reopen,
+                // protecting against late client requests that would update
+                // lastFilter and prevent normal reset.
                 clearClientSideFilterAndUpdateInMemoryFilter();
+                needsForceResetOnReopen = true;
+            } else {
+                needsForceResetOnReopen = false;
             }
         }
     }