diff --git a/src/plugins/unified_search/public/filter_bar/filter_editor/phrase_value_input.tsx b/src/plugins/unified_search/public/filter_bar/filter_editor/phrase_value_input.tsx
index 62648ae50d26a..1310ad41691c3 100644
--- a/src/plugins/unified_search/public/filter_bar/filter_editor/phrase_value_input.tsx
+++ b/src/plugins/unified_search/public/filter_bar/filter_editor/phrase_value_input.tsx
@@ -82,8 +82,10 @@ class PhraseValueInputUI extends PhraseSuggestorUI<PhraseValueInputProps> {
           onChange={([newValue = '']) => {
             onChange(newValue);
             setTimeout(() => {
-              // Note: requires a tick skip to correctly blur element focus
-              this.inputRef?.blur();
+              // Note: requires a tick skip to correctly move focus from the input to the combobox toggle
+              this.comboBoxWrapperRef.current
+                ?.querySelector<HTMLButtonElement>('[data-test-subj="comboBoxToggleListButton"]')
+                ?.focus();
             });
           }}
           onSearchChange={this.onSearchChange}
diff --git a/src/plugins/unified_search/public/filters_builder/filter_item/field_input.tsx b/src/plugins/unified_search/public/filters_builder/filter_item/field_input.tsx
index 540226caef525..eb24b392b8596 100644
--- a/src/plugins/unified_search/public/filters_builder/filter_item/field_input.tsx
+++ b/src/plugins/unified_search/public/filters_builder/filter_item/field_input.tsx
@@ -74,16 +74,13 @@ export function FieldInput({ field, dataView, onHandleField }: FieldInputProps)
     onFieldChange(newValues);
 
     setTimeout(() => {
-      // Note: requires a tick skip to correctly blur element focus
-      inputRef?.current?.blur();
+      // Note: requires a tick skip to correctly move focus from the input to the combobox toggle
+      comboBoxWrapperRef.current
+        ?.querySelector<HTMLButtonElement>('[data-test-subj="comboBoxToggleListButton"]')
+        ?.focus();
     });
   };
 
-  const handleFocus: React.FocusEventHandler<HTMLDivElement> = () => {
-    // Force focus on input due to https://github.com/elastic/eui/issues/7170
-    inputRef?.current?.focus();
-  };
-
   return (
     <div ref={comboBoxWrapperRef}>
       <EuiComboBox
@@ -101,7 +98,6 @@ export function FieldInput({ field, dataView, onHandleField }: FieldInputProps)
         isClearable={false}
         compressed
         fullWidth
-        onFocus={handleFocus}
         data-test-subj="filterFieldSuggestionList"
         singleSelection={SINGLE_SELECTION_AS_TEXT_PROPS}
         truncationProps={MIDDLE_TRUNCATION_PROPS}
diff --git a/src/plugins/unified_search/public/filters_builder/filter_item/filter_item.styles.ts b/src/plugins/unified_search/public/filters_builder/filter_item/filter_item.styles.ts
index 6ec0ac9ab7058..0fbed1f877c36 100644
--- a/src/plugins/unified_search/public/filters_builder/filter_item/filter_item.styles.ts
+++ b/src/plugins/unified_search/public/filters_builder/filter_item/filter_item.styles.ts
@@ -26,9 +26,13 @@ export const fieldAndParamCss = (euiTheme: EuiThemeComputed) => css`
   .euiFormRow {
     max-width: 800px;
   }
-  &:focus-within {
+  // Expand the combobox if the dropdown is open or the input has focus
+  &:has(input[aria-expanded='true'], input:focus) {
     flex-grow: 4;
   }
+  input {
+    width: 100% !important; // TODO: Remove this once latest EUI upgrade merges
+  }
 `;
 
 export const operationCss = (euiTheme: EuiThemeComputed) => css`
@@ -48,7 +52,7 @@ export const actionButtonCss = (euiTheme: EuiThemeComputed) => css`
 `;
 
 export const disabledDraggableCss = css`
-  &.euiDraggable .euiDraggable__item.euiDraggable__item--isDisabled {
+  &.euiDraggable .euiDraggable__item-isDisabled {
     cursor: unset;
   }
 `;