diff --git a/static/app/views/dashboards/constants.tsx b/static/app/views/dashboards/constants.tsx
index ecb766d26df4..68d9d6788b07 100644
--- a/static/app/views/dashboards/constants.tsx
+++ b/static/app/views/dashboards/constants.tsx
@@ -3,3 +3,14 @@ import {t} from 'sentry/locale';
 export const DASHBOARD_SAVING_MESSAGE = t('Saving changes\u2026');
 
 export const NUM_DESKTOP_COLS = 6;
+
+// Cache attribute-key results from the `/trace-items/attributes/` endpoint for
+// the widget builder's field pickers. Attribute keys change rarely, so a longer
+// stale time avoids re-fetching on every keystroke while searching.
+export const WIDGET_BUILDER_ATTRIBUTE_STALE_TIME = 5 * 60 * 1000;
+
+// Debounce applied to the widget builder field pickers' search input before it
+// triggers a server-side attribute fetch.
+export const WIDGET_BUILDER_ATTRIBUTE_SEARCH_DEBOUNCE_MS = 200;
+
+export const WIDGET_BUILDER_ATTRIBUTE_LOADING_MESSAGE = t('Loading…');
diff --git a/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.spec.tsx b/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.spec.tsx
new file mode 100644
index 000000000000..05d1ed056709
--- /dev/null
+++ b/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.spec.tsx
@@ -0,0 +1,98 @@
+import {OrganizationFixture} from 'sentry-fixture/organization';
+
+import {render, screen, userEvent, waitFor} from 'sentry-test/reactTestingLibrary';
+
+import {DisplayType, WidgetType} from 'sentry/views/dashboards/types';
+import {WidgetBuilderXAxisSelector} from 'sentry/views/dashboards/widgetBuilder/components/xAxisSelector';
+import {WidgetBuilderProvider} from 'sentry/views/dashboards/widgetBuilder/contexts/widgetBuilderContext';
+
+const DASHBOARD_WIDGET_BUILDER_PATHNAME =
+  '/organizations/org-slug/dashboards/new/widget/new/';
+const DASHBOARD_WIDGET_BUILDER_ROUTE = '/organizations/:orgId/dashboards/new/widget/new/';
+
+const ATTRIBUTES_URL = '/organizations/org-slug/trace-items/attributes/';
+
+const organization = OrganizationFixture({
+  features: ['performance-view', 'visibility-explore-view'],
+});
+
+const cappedAttribute = {
+  key: 'span.description',
+  name: 'span.description',
+  attributeType: 'string',
+  attributeSource: {source_type: 'sentry'},
+};
+const genAiAttribute = {
+  key: 'gen_ai.tool.name',
+  name: 'gen_ai.tool.name',
+  attributeType: 'string',
+  attributeSource: {source_type: 'sentry'},
+};
+
+describe('WidgetBuilderXAxisSelector', () => {
+  beforeEach(() => {
+    MockApiClient.addMockResponse({
+      url: ATTRIBUTES_URL,
+      method: 'GET',
+      body: [cappedAttribute],
+    });
+  });
+
+  function renderSelector() {
+    return render(
+      <WidgetBuilderProvider>
+        <WidgetBuilderXAxisSelector />
+      </WidgetBuilderProvider>,
+      {
+        organization,
+        initialRouterConfig: {
+          location: {
+            pathname: DASHBOARD_WIDGET_BUILDER_PATHNAME,
+            query: {
+              dataset: WidgetType.SPANS,
+              displayType: DisplayType.CATEGORICAL_BAR,
+            },
+          },
+          route: DASHBOARD_WIDGET_BUILDER_ROUTE,
+        },
+      }
+    );
+  }
+
+  it('fetches attributes from the server while typing', async () => {
+    const searchAttributesMock = MockApiClient.addMockResponse({
+      url: ATTRIBUTES_URL,
+      method: 'GET',
+      body: [cappedAttribute, genAiAttribute],
+      match: [MockApiClient.matchQuery({substringMatch: 'gen_ai'})],
+    });
+
+    renderSelector();
+
+    expect(await screen.findByText('X-Axis')).toBeInTheDocument();
+
+    await userEvent.click(screen.getByRole('button', {name: 'None'}));
+
+    // The attribute is not part of the initial (capped) response.
+    expect(
+      await screen.findByRole('option', {name: /span\.description/})
+    ).toBeInTheDocument();
+    expect(
+      screen.queryByRole('option', {name: /gen_ai\.tool\.name/})
+    ).not.toBeInTheDocument();
+
+    await userEvent.type(screen.getByRole('textbox'), 'gen_ai');
+
+    await waitFor(() =>
+      expect(searchAttributesMock).toHaveBeenCalledWith(
+        ATTRIBUTES_URL,
+        expect.objectContaining({
+          query: expect.objectContaining({substringMatch: 'gen_ai'}),
+        })
+      )
+    );
+    expect(
+      await screen.findByRole('option', {name: /gen_ai\.tool\.name/})
+    ).toBeInTheDocument();
+  });
+});
diff --git a/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.tsx b/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.tsx
index 5a53c09fa441..9eac5c95adf5 100644
--- a/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.tsx
+++ b/static/app/views/dashboards/widgetBuilder/components/xAxisSelector.tsx
@@ -1,4 +1,4 @@
-import {Fragment, useMemo} from 'react';
+import {Fragment, useMemo, useState} from 'react';
 import styled from '@emotion/styled';
 
 import {CompactSelect} from '@sentry/scraps/compactSelect';
@@ -7,8 +7,14 @@ import {t} from 'sentry/locale';
 import {trackAnalytics} from 'sentry/utils/analytics';
 import {WidgetBuilderVersion} from 'sentry/utils/analytics/dashboardsAnalyticsEvents';
 import {prettifyTagKey} from 'sentry/utils/fields';
+import {useDebouncedValue} from 'sentry/utils/useDebouncedValue';
 import {useOrganization} from 'sentry/utils/useOrganization';
 import {useTags} from 'sentry/utils/useTags';
+import {
+  WIDGET_BUILDER_ATTRIBUTE_LOADING_MESSAGE,
+  WIDGET_BUILDER_ATTRIBUTE_SEARCH_DEBOUNCE_MS,
+  WIDGET_BUILDER_ATTRIBUTE_STALE_TIME,
+} from 'sentry/views/dashboards/constants';
 import {getDatasetConfig} from 'sentry/views/dashboards/datasetConfig/base';
 import {WidgetType} from 'sentry/views/dashboards/types';
 import {SectionHeader} from 'sentry/views/dashboards/widgetBuilder/components/common/sectionHeader';
@@ -22,6 +28,7 @@ import {TypeBadge} from 'sentry/views/explore/components/typeBadge';
 import {HIDDEN_PREPROD_ATTRIBUTES} from 'sentry/views/explore/constants';
 import {useTraceItemDatasetAttributes} from 'sentry/views/explore/hooks/useTraceItemAttributes';
 import {HiddenTraceMetricGroupByFields} from 'sentry/views/explore/metrics/constants';
+import {sortSearchedAttributes} from 'sentry/views/explore/utils/sortSearchedAttributes';
 
 export function WidgetBuilderXAxisSelector() {
   const organization = useOrganization();
@@ -40,10 +47,32 @@ export function WidgetBuilderXAxisSelector() {
   }
 
   const {traceItemType, ...traceItemOptions} = useWidgetBuilderTraceItemConfig();
+
+  const [search, setSearch] = useState('');
+  const debouncedSearch = useDebouncedValue(
+    search,
+    WIDGET_BUILDER_ATTRIBUTE_SEARCH_DEBOUNCE_MS
+  );
+
+  const searchedTraceItemOptions = {
+    ...traceItemOptions,
+    search: debouncedSearch,
+    staleTime: WIDGET_BUILDER_ATTRIBUTE_STALE_TIME,
+  };
   const {attributes: stringSpanTags, isLoading: isLoadingStringTags} =
-    useTraceItemDatasetAttributes(traceItemType, traceItemOptions, 'string', hiddenKeys);
+    useTraceItemDatasetAttributes(
+      traceItemType,
+      searchedTraceItemOptions,
+      'string',
+      hiddenKeys
+    );
   const {attributes: numericSpanTags, isLoading: isLoadingNumericTags} =
-    useTraceItemDatasetAttributes(traceItemType, traceItemOptions, 'number', hiddenKeys);
+    useTraceItemDatasetAttributes(
+      traceItemType,
+      searchedTraceItemOptions,
+      'number',
+      hiddenKeys
+    );
 
   const datasetConfig = getDatasetConfig(state.dataset);
 
@@ -63,6 +92,7 @@ export function WidgetBuilderXAxisSelector() {
       return Object.values(allTags).map(tag => ({
         label: prettifyTagKey(tag.name),
         value: tag.key,
+        textValue: tag.key,
         trailingItems: () => <TypeBadge valueKind={FieldValueKind.TAG} />,
       }));
     }
@@ -101,6 +131,22 @@ export function WidgetBuilderXAxisSelector() {
     return fieldEntry?.field ?? '';
   }, [state.fields]);
 
+  // Keep the selected field present in the options even when it isn't in the
+  // current (possibly search-filtered) attribute response, so the dropdown
+  // reflects the saved state instead of showing nothing.
+  const fieldOptionsWithSelected = useMemo(() => {
+    if (
+      currentXAxisField &&
+      !fieldOptions.some(option => option.value === currentXAxisField)
+    ) {
+      return [
+        ...fieldOptions,
+        {label: prettifyTagKey(currentXAxisField), value: currentXAxisField},
+      ];
+    }
+    return fieldOptions;
+  }, [currentXAxisField, fieldOptions]);
+
   const handleXAxisChange = (option: {value: string | number} | undefined) => {
     if (!option) {
       return;
@@ -129,10 +175,36 @@ export function WidgetBuilderXAxisSelector() {
         tooltipText={t('Select the field to use for X-axis categories.')}
       />
       <FullWidthCompactSelect
-        search
+        search={
+          isEAPDataset
+            ? {
+                onChange: setSearch,
+                highlight: true,
+                filter: (option, searchText) =>
+                  sortSearchedAttributes({
+                    fieldDefinitionType: traceItemType,
+                    option,
+                    searchText,
+                  }),
+              }
+            : true
+        }
+        // CompactSelect clears its own search input on close but doesn't notify
+        // us, so reset our search state too. Otherwise the stale term keeps the
+        // previously fetched attributes merged into the options on reopen.
+        onOpenChange={isOpen => {
+          if (!isOpen) {
+            setSearch('');
+          }
+        }}
         loading={isLoading}
+        emptyMessage={
+          isLoading
+            ? WIDGET_BUILDER_ATTRIBUTE_LOADING_MESSAGE
+            : t('No matching attributes')
+        }
         value={currentXAxisField}
-        options={fieldOptions}
+        options={fieldOptionsWithSelected}
         onChange={handleXAxisChange}
       />
     </Fragment>