diff --git a/packages/eui/changelogs/upcoming/9142.md b/packages/eui/changelogs/upcoming/9142.md
new file mode 100644
index 00000000000..b1df289a90d
--- /dev/null
+++ b/packages/eui/changelogs/upcoming/9142.md
@@ -0,0 +1,3 @@
+**Bug fixes**
+
+- Fixed `EuiInMemoryTable` support for controlled search for plain text (when `searchFormat="text"`) by properly handling `search.query` and `search.defaulQuery`
diff --git a/packages/eui/src/components/basic_table/in_memory_table.test.tsx b/packages/eui/src/components/basic_table/in_memory_table.test.tsx
index ecd940ba313..817ceee1527 100644
--- a/packages/eui/src/components/basic_table/in_memory_table.test.tsx
+++ b/packages/eui/src/components/basic_table/in_memory_table.test.tsx
@@ -1533,7 +1533,7 @@ describe('EuiInMemoryTable', () => {
       );
       expect(mockOnChange).toHaveBeenCalledTimes(1);
       expect(mockOnChange).toHaveBeenCalledWith({
-        query: Query.parse(`"${TEXT}"`),
+        query: null,
         queryText: TEXT,
         error: null,
       });
@@ -1569,5 +1569,108 @@ describe('EuiInMemoryTable', () => {
       );
       expect(tableContent).toHaveLength(2); // 2 matches for "ba"
     });
+
+    it('supports controlled operation, query is reflected in the search box', () => {
+      const items = [{ title: 'foo' }, { title: 'bar' }, { title: 'baz' }];
+      const columns = [{ field: 'title', name: 'Title' }];
+      const CONTROLLED_QUERY = 'controlled search';
+
+      const { getByTestSubject, rerender } = render(
+        <EuiInMemoryTable
+          items={items}
+          searchFormat="text"
+          search={{
+            query: CONTROLLED_QUERY,
+            box: { incremental: true, 'data-test-subj': 'searchbox' },
+          }}
+          columns={columns}
+        />
+      );
+
+      const searchbox = getByTestSubject('searchbox') as HTMLInputElement;
+      expect(searchbox.value).toBe(CONTROLLED_QUERY);
+
+      // Update the controlled query
+      const UPDATED_QUERY = 'updated search';
+      rerender(
+        <EuiInMemoryTable
+          items={items}
+          searchFormat="text"
+          search={{
+            query: UPDATED_QUERY,
+            box: { incremental: true, 'data-test-subj': 'searchbox' },
+          }}
+          columns={columns}
+        />
+      );
+
+      expect(searchbox.value).toBe(UPDATED_QUERY);
+    });
+
+    it('renders defaultQuery in the search box on initial render', () => {
+      const items = [{ title: 'foo' }, { title: 'bar' }, { title: 'baz' }];
+      const columns = [{ field: 'title', name: 'Title' }];
+      const DEFAULT_QUERY = 'default search text';
+
+      const { getByTestSubject } = render(
+        <EuiInMemoryTable
+          items={items}
+          searchFormat="text"
+          search={{
+            defaultQuery: DEFAULT_QUERY,
+            box: { incremental: true, 'data-test-subj': 'searchbox' },
+          }}
+          columns={columns}
+        />
+      );
+
+      const searchbox = getByTestSubject('searchbox') as HTMLInputElement;
+
+      expect(searchbox.value).toBe(DEFAULT_QUERY);
+
+      fireEvent.keyUp(searchbox, {
+        target: { value: 'something else' },
+      });
+
+      expect(searchbox.value).toBe('something else');
+    });
+
+    it('ignores Query objects in the search box', () => {
+      const items = [{ title: 'foo' }, { title: 'bar' }, { title: 'baz' }];
+      const columns = [{ field: 'title', name: 'Title' }];
+      const query = Query.parse('ba');
+
+      const { getByTestSubject, rerender } = render(
+        <EuiInMemoryTable
+          items={items}
+          searchFormat="text"
+          search={{
+            query,
+            box: { incremental: true, 'data-test-subj': 'searchbox' },
+          }}
+          columns={columns}
+        />
+      );
+
+      const searchbox = getByTestSubject('searchbox') as HTMLInputElement;
+
+      // not `[object Object]`
+      expect(searchbox.value).toBe('');
+
+      rerender(
+        <EuiInMemoryTable
+          items={items}
+          searchFormat="text"
+          search={{
+            defaultQuery: query,
+            box: { incremental: true, 'data-test-subj': 'searchbox' },
+          }}
+          columns={columns}
+        />
+      );
+
+      // not `[object Object]`
+      expect(searchbox.value).toBe('');
+    });
   });
 });
diff --git a/packages/eui/src/components/basic_table/in_memory_table.tsx b/packages/eui/src/components/basic_table/in_memory_table.tsx
index 03d636e1110..5ac3b93fd9d 100644
--- a/packages/eui/src/components/basic_table/in_memory_table.tsx
+++ b/packages/eui/src/components/basic_table/in_memory_table.tsx
@@ -85,7 +85,11 @@ type InMemoryTableProps<T extends object> = Omit<
    */
   noItemsMessage?: ReactNode;
   /**
-   * Configures {@link Search}.
+   * Configures the search bar. Can be `true` for defaults,
+   * or an {@link EuiSearchBarProps} object.
+   *
+   * When `searchFormat="text"`, `query` and `defaultQuery` must be strings
+   * ({@link Query} objects are ignored).
    */
   search?: Search;
   /**
@@ -93,6 +97,7 @@ type InMemoryTableProps<T extends object> = Omit<
    *
    * However, certain special characters (such as quotes, parentheses, and colons)
    * are reserved for EQL syntax and will error if used.
+   *
    * If your table does not require filter search and instead requires searching for certain
    * symbols, use a plain `text` search format instead (note that filters will be ignored
    * in this format).
@@ -159,7 +164,7 @@ interface State<T extends object> {
     search?: Search;
   };
   search?: Search;
-  query: Query | null;
+  query: Query | string | null;
   pageIndex: number;
   pageSize?: number;
   pageSizeOptions?: number[];
@@ -169,23 +174,34 @@ interface State<T extends object> {
   showPerPageOptions: boolean | undefined;
 }
 
+/**
+ * Extracts and formats a query from search props based on the search format
+ * @param search - The search configuration
+ * @param defaultQuery - Whether to use the defaultQuery property as fallback
+ * @param searchFormat - The search format: 'eql' for parsed queries, 'text' for plain text
+ * @returns Formatted query string or Query object
+ */
 const getQueryFromSearch = (
   search: Search | undefined,
-  defaultQuery: boolean
-) => {
-  let query: Query | string;
+  defaultQuery: boolean,
+  searchFormat: InMemoryTableProps<{}>['searchFormat']
+): Query | string => {
   if (!search) {
-    query = '';
-  } else {
-    query =
-      (defaultQuery
-        ? (search as EuiSearchBarProps).defaultQuery ||
-          (search as EuiSearchBarProps).query ||
-          ''
-        : (search as EuiSearchBarProps).query) || '';
+    return searchFormat === 'text' ? '""' : '';
+  }
+
+  const searchProps = search as EuiSearchBarProps;
+  const queryString = defaultQuery
+    ? searchProps.defaultQuery ?? searchProps.query ?? ''
+    : searchProps.query ?? '';
+
+  if (searchFormat === 'text') {
+    return `"${queryString}"`;
   }
 
-  return isString(query) ? EuiSearchBar.Query.parse(query) : query;
+  return isString(queryString)
+    ? EuiSearchBar.Query.parse(queryString)
+    : queryString;
 };
 
 const getInitialPagination = (
@@ -398,7 +414,11 @@ export class EuiInMemoryTable<T extends object = object> extends Component<
           ...updatedPrevState.prevProps,
           search: nextProps.search,
         },
-        query: getQueryFromSearch(nextProps.search, false),
+        query: getQueryFromSearch(
+          nextProps.search,
+          false,
+          nextProps.searchFormat ?? 'eql'
+        ),
       };
     }
     if (updatedPrevState !== prevState) {
@@ -423,7 +443,7 @@ export class EuiInMemoryTable<T extends object = object> extends Component<
         search,
       },
       search: search,
-      query: getQueryFromSearch(search, true),
+      query: getQueryFromSearch(search, true, props.searchFormat ?? 'eql'),
       pageIndex: pageIndex || 0,
       pageSize,
       pageSizeOptions,
@@ -542,13 +562,12 @@ export class EuiInMemoryTable<T extends object = object> extends Component<
   // search bar to ignore EQL syntax and only use the searchbar for plain text
   onPlainTextSearch = (searchValue: string) => {
     const escapedQueryText = searchValue.replace(/["\\]/g, '\\$&');
-    const finalQuery = `"${escapedQueryText}"`;
     const { search } = this.props;
 
     if (isEuiSearchBarProps(search)) {
       if (search.onChange) {
         const shouldQueryInMemory = search.onChange({
-          query: EuiSearchBar.Query.parse(finalQuery),
+          query: null,
           queryText: escapedQueryText,
           error: null,
         });
@@ -559,7 +578,7 @@ export class EuiInMemoryTable<T extends object = object> extends Component<
     }
 
     this.setState({
-      query: EuiSearchBar.Query.parse(finalQuery),
+      query: `"${escapedQueryText}"`,
     });
   };
 
@@ -570,13 +589,37 @@ export class EuiInMemoryTable<T extends object = object> extends Component<
     let searchBar: ReactNode;
 
     if (searchFormat === 'text') {
-      const _searchBoxProps = (search as EuiSearchBarProps)?.box || {}; // Work around | boolean type
-      const { schema, ...searchBoxProps } = _searchBoxProps; // Destructure `schema` so it doesn't get rendered to DOM
+      const { box = {}, query, defaultQuery } = search as EuiSearchBarProps;
+      const {
+        schema, // destructure `schema` so it doesn't get rendered to DOM
+        ...searchBoxProps
+      } = box;
+
+      // in the unexpected case a Query object is passed with searchFormat=text
+      if (process.env.NODE_ENV === 'development') {
+        if (query != null && !isString(query)) {
+          console.warn(
+            'EuiInMemoryTable: `query` should be a string when using searchFormat="text". Query objects are only supported with searchFormat="eql".'
+          );
+        }
+        if (defaultQuery != null && !isString(defaultQuery)) {
+          console.warn(
+            'EuiInMemoryTable: `defaultQuery` should be a string when using searchFormat="text". Query objects are only supported with searchFormat="eql".'
+          );
+        }
+      }
+
+      // use only string values, ignore Query objects
+      const displayQuery = isString(query)
+        ? query
+        : isString(defaultQuery)
+        ? defaultQuery
+        : '';
 
       searchBar = (
         <EuiSearchBox
-          query="" // Unused, passed to satisfy Typescript
           {...searchBoxProps}
+          query={displayQuery}
           onSearch={this.onPlainTextSearch}
         />
       );
diff --git a/packages/eui/src/components/search_bar/search_bar.tsx b/packages/eui/src/components/search_bar/search_bar.tsx
index ed4f5da1ba1..c57ce764fd2 100644
--- a/packages/eui/src/components/search_bar/search_bar.tsx
+++ b/packages/eui/src/components/search_bar/search_bar.tsx
@@ -34,6 +34,16 @@ interface ArgsWithQuery {
   error: null;
 }
 
+/**
+ * When `searchFormat` is 'text', `query` is null and the search is performed
+ * on the `queryText` directly without EQL parsing
+ */
+interface ArgsWithPlainText {
+  query: null;
+  queryText: string;
+  error: null;
+}
+
 interface ArgsWithError {
   query: null;
   queryText: string;
@@ -48,7 +58,10 @@ export interface SchemaType {
   recognizedFields?: string[];
 }
 
-export type EuiSearchBarOnChangeArgs = ArgsWithQuery | ArgsWithError;
+export type EuiSearchBarOnChangeArgs =
+  | ArgsWithQuery
+  | ArgsWithPlainText
+  | ArgsWithError;
 
 type HintPopOverProps = Partial<
   Pick<
@@ -72,17 +85,17 @@ export interface EuiSearchBarProps extends CommonProps {
   onChange?: (args: EuiSearchBarOnChangeArgs) => void | boolean;
 
   /**
-   The initial query the bar will hold when first mounted
+   * The initial query the bar will hold when first mounted
    */
   defaultQuery?: QueryType;
 
   /**
-   If you wish to use the search bar as a controlled component, continuously pass the query via this prop.
+   * If you wish to use the search bar as a controlled component, continuously pass the query via this prop.
    */
   query?: QueryType;
 
   /**
-   Configures the search box. Set `placeholder` to change the placeholder text in the box and `incremental` to support incremental (as you type) search.
+   * Configures the search box. Set `placeholder` to change the placeholder text in the box and `incremental` to support incremental (as you type) search.
    */
   box?: EuiFieldSearchProps & {
     // Boolean values are not meaningful to this EuiSearchBox, but are allowed so that other
@@ -92,7 +105,7 @@ export interface EuiSearchBarProps extends CommonProps {
   };
 
   /**
-   An array of search filters. See {@link SearchFilterConfig}.
+   * An array of search filters. See {@link SearchFilterConfig}.
    */
   filters?: SearchFilterConfig[];