diff --git a/tools/test-js-with-node b/tools/test-js-with-node
index 7febdb6368..15335e25d4 100755
--- a/tools/test-js-with-node
+++ b/tools/test-js-with-node
@@ -121,6 +121,7 @@ EXEMPT_FILES = make_set(
         "web/src/inbox_util.ts",
         "web/src/info_overlay.ts",
         "web/src/information_density.ts",
+        "web/src/input_pill.ts",
         "web/src/integration_url_modal.ts",
         "web/src/invite.ts",
         "web/src/invite_stream_picker_pill.ts",
@@ -199,6 +200,7 @@ EXEMPT_FILES = make_set(
         "web/src/scroll_util.ts",
         "web/src/search.ts",
         "web/src/search_pill.ts",
+        "web/src/search_suggestion.ts",
         "web/src/sent_messages.ts",
         "web/src/sentry.ts",
         "web/src/server_events.js",
diff --git a/web/src/input_pill.ts b/web/src/input_pill.ts
index 0ad2cde20e..910853f26a 100644
--- a/web/src/input_pill.ts
+++ b/web/src/input_pill.ts
@@ -4,10 +4,12 @@ import $ from "jquery";
 import assert from "minimalistic-assert";
 
 import render_input_pill from "../templates/input_pill.hbs";
+import render_search_user_pill from "../templates/search_user_pill.hbs";
 
 import * as blueslip from "./blueslip";
 import type {EmojiRenderingDetails} from "./emoji";
 import * as keydown_util from "./keydown_util";
+import type {SearchUserPill} from "./search_pill";
 import * as ui_util from "./ui_util";
 
 // See https://zulip.readthedocs.io/en/latest/subsystems/input-pills.html
@@ -21,6 +23,8 @@ export type InputPillItem<T> = {
     should_add_guest_user_indicator?: boolean;
     user_id?: number;
     group_id?: number;
+    // Used for search pills
+    operator?: string;
 } & T;
 
 export type InputPillConfig = {
@@ -158,36 +162,39 @@ export function create<T>(opts: InputPillCreateOptions<T>): InputPillContainer<T
                 blueslip.error("no type defined for the item");
                 return;
             }
+            let pill_html;
+            if (item.type === "search_user") {
+                pill_html = render_search_user_pill(item);
+            } else {
+                const has_image = item.img_src !== undefined;
 
-            const has_image = item.img_src !== undefined;
+                const opts: InputPillRenderingDetails = {
+                    display_value: item.display_value,
+                    has_image,
+                    deactivated: item.deactivated,
+                    should_add_guest_user_indicator: item.should_add_guest_user_indicator,
+                };
 
-            const opts: InputPillRenderingDetails = {
-                display_value: item.display_value,
-                has_image,
-                deactivated: item.deactivated,
-                should_add_guest_user_indicator: item.should_add_guest_user_indicator,
-            };
-
-            if (item.user_id) {
-                opts.user_id = item.user_id;
-            }
-            if (item.group_id) {
-                opts.group_id = item.group_id;
-            }
-
-            if (has_image) {
-                opts.img_src = item.img_src;
-            }
-
-            if (store.pill_config?.show_user_status_emoji === true) {
-                const has_status = item.status_emoji_info !== undefined;
-                if (has_status) {
-                    opts.status_emoji_info = item.status_emoji_info;
+                if (item.user_id) {
+                    opts.user_id = item.user_id;
+                }
+                if (item.group_id) {
+                    opts.group_id = item.group_id;
                 }
-                opts.has_status = has_status;
-            }
 
-            const pill_html = render_input_pill(opts);
+                if (has_image) {
+                    opts.img_src = item.img_src;
+                }
+
+                if (store.pill_config?.show_user_status_emoji === true) {
+                    const has_status = item.status_emoji_info !== undefined;
+                    if (has_status) {
+                        opts.status_emoji_info = item.status_emoji_info;
+                    }
+                    opts.has_status = has_status;
+                }
+                pill_html = render_input_pill(opts);
+            }
             const payload: InputPill<T> = {
                 item,
                 $element: $(pill_html),
@@ -249,6 +256,59 @@ export function create<T>(opts: InputPillCreateOptions<T>): InputPillContainer<T
             return undefined;
         },
 
+        // TODO: This function is only used for the search input supporting multiple user
+        // pills within an individual top-level pill. Ideally, we'd encapsulate it in a
+        // subclass used only for search so that this code can be part of search_pill.ts.
+        removeUserPill(user_container: HTMLElement, user_id: number) {
+            // First get the outer pill that contains the user pills.
+            let container_idx: number | undefined;
+            for (let x = 0; x < store.pills.length; x += 1) {
+                if (store.pills[x]!.$element[0] === user_container) {
+                    container_idx = x;
+                }
+            }
+            assert(container_idx !== undefined);
+            assert(store.pills[container_idx]!.item.type === "search_user");
+            // TODO: Figure out how to get this typed correctly.
+            // eslint-disable-next-line @typescript-eslint/consistent-type-assertions
+            const user_pill_container = store.pills[container_idx]!
+                .item as unknown as InputPillItem<SearchUserPill>;
+
+            // If there's only one user in this pill, delete the whole pill.
+            if (user_pill_container.users.length === 1) {
+                assert(user_pill_container.users[0]!.user_id === user_id);
+                this.removePill(user_container);
+                return;
+            }
+
+            // Remove the user id from the pill data.
+            let user_idx: number | undefined;
+            for (let x = 0; x < user_pill_container.users.length; x += 1) {
+                if (user_pill_container.users[x]!.user_id === user_id) {
+                    user_idx = x;
+                }
+            }
+            assert(user_idx !== undefined);
+            user_pill_container.users.splice(user_idx, 1);
+            const sign = user_pill_container.negated ? "-" : "";
+            const search_string =
+                sign +
+                user_pill_container.operator +
+                ":" +
+                user_pill_container.users.map((user) => user.email).join(",");
+            user_pill_container.display_value = search_string;
+
+            // Remove the user pill from the DOM.
+            const $user_pill = $(store.pills[container_idx]!.$element.children(".pill")[user_idx]!);
+            assert($user_pill.data("user-id") === user_id);
+            $user_pill.remove();
+
+            // This is needed to run the "change" event handler registered in
+            // compose_recipient.js, which calls the `update_on_recipient_change` to update
+            // the compose_fade state.
+            store.$input.trigger("change");
+        },
+
         // this will remove the last pill in the container -- by default tied
         // to the "Backspace" key when the value of the input is empty.
         // If quiet is a truthy value, the event handler associated with the
@@ -444,6 +504,18 @@ export function create<T>(opts: InputPillCreateOptions<T>): InputPillContainer<T
         // when the "×" is clicked on a pill, it should delete that pill and then
         // select the next pill (or input).
         store.$parent.on("click", ".exit", function (this: HTMLElement, e) {
+            const $user_pill_container = $(this).parents(".user-pill-container");
+            if ($user_pill_container.length) {
+                // The user-pill-container container class is used exclusively for
+                // group-DM search pills, where multiple user pills sit inside a larger
+                // pill. The exit icons in those individual user pills should remove
+                // just that pill, not the outer pill.
+                // TODO: Figure out how to move this code into search_pill.ts.
+                const user_id = $(this).closest(".pill").attr("data-user-id");
+                assert(user_id !== undefined);
+                funcs.removeUserPill($user_pill_container[0]!, Number.parseInt(user_id, 10));
+                return;
+            }
             e.stopPropagation();
             const $pill = $(this).closest(".pill");
             const $next = $pill.next();
diff --git a/web/src/search.ts b/web/src/search.ts
index ff66be459e..49eafbc92c 100644
--- a/web/src/search.ts
+++ b/web/src/search.ts
@@ -83,6 +83,10 @@ export function initialize({on_narrow_search}: {on_narrow_search: OnNarrowSearch
         search_input_has_changed = true;
     });
 
+    $search_query_box.on("change", () => {
+        search_typeahead.lookup(false);
+    });
+
     // Data storage for the typeahead.
     // This maps a search string to an object with a "description_html" field.
     // (It's a bit of legacy that we have an object with only one important
diff --git a/web/src/search_pill.ts b/web/src/search_pill.ts
index 0213727f9b..1f811fa483 100644
--- a/web/src/search_pill.ts
+++ b/web/src/search_pill.ts
@@ -1,13 +1,42 @@
+import assert from "minimalistic-assert";
+
 import {Filter} from "./filter";
 import * as input_pill from "./input_pill";
 import type {InputPillContainer} from "./input_pill";
+import * as people from "./people";
+import type {User} from "./people";
 import type {NarrowTerm} from "./state_data";
+import * as user_status from "./user_status";
+import type {UserStatusEmojiInfo} from "./user_status";
 
-type SearchPill = {
+export type SearchUserPill = {
+    type: "search_user";
+    operator: string;
+    // TODO: It would be nice if we just call this `search_string` instead of
+    // `display_value`, because we don't actually display this value for user
+    // pills, but `display_value` is needed to hook into the generic input pill
+    // logic and it would be a decent amount of work to change that.
     display_value: string;
-    type: string;
-    description_html: string;
+    negated: boolean;
+    users: {
+        display_value: string;
+        user_id: number;
+        email: string;
+        img_src: string;
+        status_emoji_info: UserStatusEmojiInfo | undefined;
+        should_add_guest_user_indicator: boolean;
+        deactivated: boolean;
+    }[];
 };
+
+type SearchPill =
+    | {
+          type: "search";
+          display_value: string;
+          description_html: string;
+      }
+    | SearchUserPill;
+
 export type SearchPillWidget = InputPillContainer<SearchPill>;
 
 export function create_item_from_search_string(search_string: string): SearchPill {
@@ -34,6 +63,36 @@ export function create_pills($pill_container: JQuery): SearchPillWidget {
     return pills;
 }
 
+function append_user_pill(
+    users: User[],
+    pill_widget: SearchPillWidget,
+    operator: string,
+    negated: boolean,
+): void {
+    const sign = negated ? "-" : "";
+    const search_string = sign + operator + ":" + users.map((user) => user.email).join(",");
+    const pill_data: SearchUserPill = {
+        type: "search_user",
+        operator,
+        display_value: search_string,
+        negated,
+        users: users.map((user) => ({
+            display_value: user.full_name,
+            user_id: user.user_id,
+            email: user.email,
+            img_src: people.small_avatar_url_for_person(user),
+            status_emoji_info: user_status.get_status_emoji(user.user_id),
+            should_add_guest_user_indicator: people.should_add_guest_user_indicator(user.user_id),
+            deactivated: !people.is_person_active(user.user_id) && !user.is_inaccessible_user,
+        })),
+    };
+
+    pill_widget.appendValidatedData(pill_data);
+    pill_widget.clear_text();
+}
+
+const user_pill_operators = new Set(["dm", "dm-including", "sender"]);
+
 export function set_search_bar_contents(
     search_terms: NarrowTerm[],
     pill_widget: SearchPillWidget,
@@ -42,6 +101,16 @@ export function set_search_bar_contents(
     pill_widget.clear();
     let partial_pill = "";
     for (const term of search_terms) {
+        if (user_pill_operators.has(term.operator) && term.operand !== "") {
+            const user_emails = term.operand.split(",");
+            const users = user_emails.map((email) => {
+                const user = people.get_by_email(email);
+                assert(user !== undefined);
+                return user;
+            });
+            append_user_pill(users, pill_widget, term.operator, term.negated ?? false);
+            continue;
+        }
         const input = Filter.unparse([term]);
         // If the last term looks something like `dm:`, we
         // don't want to make it a pill, since it isn't isn't
diff --git a/web/src/search_suggestion.ts b/web/src/search_suggestion.ts
index 786ba049fd..8e5065d899 100644
--- a/web/src/search_suggestion.ts
+++ b/web/src/search_suggestion.ts
@@ -181,9 +181,40 @@ function get_channel_suggestions(last: NarrowTerm, terms: NarrowTerm[]): Suggest
 }
 
 function get_group_suggestions(last: NarrowTerm, terms: NarrowTerm[]): Suggestion[] {
+    // We only suggest groups once a term with a valid user already exists
+    if (terms.length === 0) {
+        return [];
+    }
+    const last_complete_term = terms.at(-1)!;
     // For users with "pm-with" in their muscle memory, still
     // have group direct message suggestions with "dm:" operator.
-    if (!check_validity(last, terms, ["dm", "pm-with"], [{operator: "channel"}])) {
+    if (
+        !check_validity(
+            last_complete_term,
+            terms.slice(-1),
+            ["dm", "pm-with"],
+            [{operator: "channel"}],
+        )
+    ) {
+        return [];
+    }
+
+    // If they started typing since a user pill, we'll parse that as "search"
+    // but they might actually want to parse that as a user instead to add to
+    // the most recent pill. So we shuffle some things around to support that.
+    if (last.operator === "search") {
+        const text_input = last.operand;
+        const operand = `${last_complete_term.operand},${text_input}`;
+        last = {
+            ...last_complete_term,
+            operand,
+        };
+        terms = terms.slice(-1);
+    } else if (last.operator === "") {
+        last = last_complete_term;
+    } else {
+        // If they already started another term with an other operator, we're
+        // no longer dealing with a group DM situation.
         return [];
     }
 
@@ -197,14 +228,17 @@ function get_group_suggestions(last: NarrowTerm, terms: NarrowTerm[]): Suggestio
     // we only use the last part to generate suggestions.
 
     const last_comma_index = operand.lastIndexOf(",");
+    let all_but_last_part;
+    let last_part;
     if (last_comma_index < 0) {
-        return [];
+        all_but_last_part = operand;
+        last_part = "";
+    } else {
+        // Neither all_but_last_part nor last_part include the final comma.
+        all_but_last_part = operand.slice(0, last_comma_index);
+        last_part = operand.slice(last_comma_index + 1);
     }
 
-    // Neither all_but_last_part nor last_part include the final comma.
-    const all_but_last_part = operand.slice(0, last_comma_index);
-    const last_part = operand.slice(last_comma_index + 1);
-
     // We don't suggest a person if their email is already present in the
     // operand (not including the last part).
     const parts = [...all_but_last_part.split(","), people.my_current_email()];
@@ -827,7 +861,24 @@ class Attacher {
 
     attach_many(suggestions: Suggestion[]): void {
         for (const suggestion of suggestions) {
-            const suggestion_line = [...this.base, suggestion];
+            let suggestion_line;
+            if (this.base.length === 0) {
+                suggestion_line = [suggestion];
+            } else {
+                // When we add a user to a user group, we
+                // replace the last pill.
+                const last_base_term = this.base.at(-1)!;
+                const last_base_string = last_base_term.search_string;
+                const new_search_string = suggestion.search_string;
+                if (
+                    new_search_string.startsWith("dm:") &&
+                    new_search_string.includes(last_base_string)
+                ) {
+                    suggestion_line = [...this.base.slice(0, -1), suggestion];
+                } else {
+                    suggestion_line = [...this.base, suggestion];
+                }
+            }
             this.push(suggestion_line);
         }
     }
@@ -949,15 +1000,19 @@ export function get_search_result(query_from_pills: string, query_from_text: str
 
     // Remember to update the spectator list when changing this.
     let filterers = [
+        // This should show before other `get_people` suggestions
+        // because both are valid suggestions for typing a user's
+        // name, and if there's already has a DM pill then the
+        // searching user probably is looking to make a group DM.
+        get_group_suggestions,
         get_channels_filter_suggestions,
         get_is_filter_suggestions,
         get_sent_by_me_suggestions,
         get_channel_suggestions,
-        get_people("sender"),
         get_people("dm"),
+        get_people("sender"),
         get_people("dm-including"),
         get_people("from"),
-        get_group_suggestions,
         get_topic_suggestions,
         get_operator_suggestions,
         get_has_filter_suggestions,
diff --git a/web/styles/app_variables.css b/web/styles/app_variables.css
index 1bf85e5e1d..90e7f74a74 100644
--- a/web/styles/app_variables.css
+++ b/web/styles/app_variables.css
@@ -567,6 +567,7 @@
     --color-background-exit-hover-deactivated-user-pill: hsl(
         4deg 75% 53% / 15%
     );
+    --color-background-user-pill: hsla(0deg 0% 100% / 85%);
 
     /* Inbox view constants - Values from Figma design */
     --height-inbox-search: 26px;
@@ -949,6 +950,7 @@
     --color-focus-outline-deactivated-user-pill: hsl(0deg 0% 100% / 70%);
     --color-close-deactivated-user-pill: hsl(7deg 100% 74%);
     --color-background-exit-hover-deactivated-user-pill: hsl(0deg 0% 100% / 7%);
+    --color-background-user-pill: hsl(0deg 0% 0% / 40%);
 
     /* Inbox view */
     --color-background-inbox: var(--color-background);
diff --git a/web/styles/search.css b/web/styles/search.css
index fa9762cdd8..457ee5c604 100644
--- a/web/styles/search.css
+++ b/web/styles/search.css
@@ -68,7 +68,7 @@
     .search-input-and-pills {
         grid-area: search-pills;
         display: flex;
-        padding: 3px 0;
+        padding: 0;
         flex-wrap: wrap;
         gap: 2px 2px;
         align-self: center;
@@ -222,6 +222,7 @@
         .pill {
             margin: 0;
             min-width: unset;
+            height: 26px;
         }
 
         &:not(.focused) {
@@ -233,6 +234,33 @@
                 overflow: hidden;
             }
         }
+
+        .user-pill-container {
+            padding: 2px;
+            height: 22px;
+            min-width: fit-content;
+
+            > .pill-label {
+                min-width: fit-content;
+                white-space: nowrap;
+                width: fit-content;
+            }
+
+            .pill {
+                height: 22px;
+                margin: 2px;
+                border: none;
+
+                &:not(.deactivated-pill) {
+                    background-color: var(--color-background-user-pill);
+                }
+            }
+
+            .pill-image {
+                width: 22px;
+                height: 22px;
+            }
+        }
     }
 
     @media (width >= $md_min) {
diff --git a/web/templates/search_user_pill.hbs b/web/templates/search_user_pill.hbs
new file mode 100644
index 0000000000..6a5ba322a3
--- /dev/null
+++ b/web/templates/search_user_pill.hbs
@@ -0,0 +1,22 @@
+<div class="user-pill-container pill" tabindex=0>
+    <span class="pill-label">
+        {{~#if this.negated}}-{{~/if~}}
+        {{ operator }}:
+    </span>
+    {{#each users}}
+        <div class="pill{{#if deactivated}} deactivated-pill{{/if}}" data-user-id="{{this.user_id}}">
+            <img class="pill-image" src="{{this.img_src}}" />
+            <span class="pill-label">
+                <span class="pill-value">{{ this.display_value }}</span>
+                {{~#if this.should_add_guest_user_indicator}}&nbsp;<i>({{t 'guest'}})</i>{{~/if~}}
+                {{~#if deactivated}}&nbsp;({{t 'deactivated'}}){{~/if~}}
+                {{~#if this.status_emoji_info~}}
+                    {{~> status_emoji this.status_emoji_info~}}
+                {{~/if~}}
+            </span>
+            <div class="exit">
+                <a role="button" class="zulip-icon zulip-icon-close pill-close-button"></a>
+            </div>
+        </div>
+    {{/each}}
+</div>
diff --git a/web/tests/input_pill.test.js b/web/tests/input_pill.test.js
index 55bb0d276f..ab2e85d8b7 100644
--- a/web/tests/input_pill.test.js
+++ b/web/tests/input_pill.test.js
@@ -529,6 +529,9 @@ run_test("exit button on pill", ({mock_template}) => {
                 assert.equal(sel, ".pill");
                 return $curr_pill_stub;
             },
+            parents() {
+                return [];
+            },
         }),
     };
 
diff --git a/web/tests/search_suggestion.test.js b/web/tests/search_suggestion.test.js
index 4e1802e80a..b44b9d02bc 100644
--- a/web/tests/search_suggestion.test.js
+++ b/web/tests/search_suggestion.test.js
@@ -68,8 +68,8 @@ function init() {
     stream_data.clear_subscriptions();
 }
 
-function get_suggestions(query) {
-    return search.get_suggestions("", query);
+function get_suggestions(query, pill_query = "") {
+    return search.get_suggestions(pill_query, query);
 }
 
 function test(label, f) {
@@ -151,8 +151,8 @@ test("dm_suggestions", ({override, mock_template}) => {
     expected = [
         "is:dm al",
         "is:dm is:alerted",
-        "is:dm sender:alice@zulip.com",
         "is:dm dm:alice@zulip.com",
+        "is:dm sender:alice@zulip.com",
         "is:dm dm-including:alice@zulip.com",
         "is:dm",
     ];
@@ -234,8 +234,8 @@ test("dm_suggestions", ({override, mock_template}) => {
     expected = [
         "is:starred has:link is:dm al",
         "is:starred has:link is:dm is:alerted",
-        "is:starred has:link is:dm sender:alice@zulip.com",
         "is:starred has:link is:dm dm:alice@zulip.com",
+        "is:starred has:link is:dm sender:alice@zulip.com",
         "is:starred has:link is:dm dm-including:alice@zulip.com",
         "is:starred has:link is:dm",
         "is:starred has:link",
@@ -272,90 +272,73 @@ test("group_suggestions", ({mock_template}) => {
     mock_template("search_description.hbs", true, (_data, html) => html);
     mock_template("user_pill.hbs", true, (_data, html) => html);
 
-    // Entering a comma in a "dm:" query should immediately
-    // generate suggestions for the next person.
-    let query = "dm:bob@zulip.com,";
-    let suggestions = get_suggestions(query);
+    // If there's an existing completed user pill right before
+    // the input string, we suggest a user group as one of the
+    // suggestions.
+    let pill_query = "dm:bob@zulip.com";
+    let query = "alice";
+    let suggestions = get_suggestions(query, pill_query);
     let expected = [
-        "dm:bob@zulip.com,",
+        "dm:bob@zulip.com alice",
         "dm:bob@zulip.com,alice@zulip.com",
-        "dm:bob@zulip.com,jeff@zulip.com",
-        "dm:bob@zulip.com,ted@zulip.com",
+        "dm:bob@zulip.com sender:alice@zulip.com",
+        "dm:bob@zulip.com dm-including:alice@zulip.com",
+        "dm:bob@zulip.com",
     ];
     assert.deepEqual(suggestions.strings, expected);
 
-    // Only the last part of a comma-separated "dm" query
-    // should be used to generate suggestions.
-    query = "dm:bob@zulip.com,t";
-    suggestions = get_suggestions(query);
-    expected = ["dm:bob@zulip.com,t", "dm:bob@zulip.com,ted@zulip.com"];
-    assert.deepEqual(suggestions.strings, expected);
-
-    // Smit should also generate ted@zulip.com (Ted Smith) as a suggestion.
-    query = "dm:bob@zulip.com,Smit";
-    suggestions = get_suggestions(query);
-    expected = ["dm:bob@zulip.com,Smit", "dm:bob@zulip.com,ted@zulip.com"];
-    assert.deepEqual(suggestions.strings, expected);
-
-    // Do not suggest "myself@zulip.com" (the name of the current user)
-    query = "dm:ted@zulip.com,my";
-    suggestions = get_suggestions(query);
-    expected = ["dm:ted@zulip.com,my"];
-    assert.deepEqual(suggestions.strings, expected);
-
-    // No superfluous suggestions should be generated.
-    query = "dm:bob@zulip.com,red";
-    suggestions = get_suggestions(query);
-    expected = ["dm:bob@zulip.com,red"];
+    // Do not suggest "myself@zulip.com" (the name of the current user) for dms
+    pill_query = "dm:ted@zulip.com";
+    query = "my";
+    suggestions = get_suggestions(query, pill_query);
+    expected = [
+        "dm:ted@zulip.com my",
+        "dm:ted@zulip.com sender:myself@zulip.com",
+        "dm:ted@zulip.com dm-including:myself@zulip.com",
+        "dm:ted@zulip.com",
+    ];
     assert.deepEqual(suggestions.strings, expected);
 
     // "is:dm" should be properly prepended to each suggestion
     // if the "dm" operator is negated.
 
-    query = "-dm:bob@zulip.com,";
+    query = "-dm:bob@zulip.co";
     suggestions = get_suggestions(query);
     expected = [
-        "-dm:bob@zulip.com,",
-        "is:dm -dm:bob@zulip.com,alice@zulip.com",
-        "is:dm -dm:bob@zulip.com,jeff@zulip.com",
-        "is:dm -dm:bob@zulip.com,ted@zulip.com",
+        "-dm:bob@zulip.co",
+        "is:dm -dm:bob@zulip.com",
     ];
     assert.deepEqual(suggestions.strings, expected);
 
-    query = "-dm:bob@zulip.com,t";
-    suggestions = get_suggestions(query);
-    expected = ["-dm:bob@zulip.com,t", "is:dm -dm:bob@zulip.com,ted@zulip.com"];
-    assert.deepEqual(suggestions.strings, expected);
-
-    query = "-dm:bob@zulip.com,Smit";
-    suggestions = get_suggestions(query);
-    expected = ["-dm:bob@zulip.com,Smit", "is:dm -dm:bob@zulip.com,ted@zulip.com"];
-    assert.deepEqual(suggestions.strings, expected);
-
     query = "-dm:bob@zulip.com,red";
     suggestions = get_suggestions(query);
     expected = ["-dm:bob@zulip.com,red"];
     assert.deepEqual(suggestions.strings, expected);
 
-    // If user types "pm-with" operator, an email and a comma,
-    // show suggestions for group direct messages with the "dm"
-    // operator.
-    query = "pm-with:bob@zulip.com,";
-    suggestions = get_suggestions(query);
+    // If user types "pm-with" operator, show suggestions for
+    // group direct messages with the "dm" operator.
+    pill_query = "pm-with:bob@zulip.com";
+    query = "alice";
+    suggestions = get_suggestions(query, pill_query);
     expected = [
-        "dm:bob@zulip.com,",
+        "dm:bob@zulip.com alice",
         "dm:bob@zulip.com,alice@zulip.com",
-        "dm:bob@zulip.com,jeff@zulip.com",
-        "dm:bob@zulip.com,ted@zulip.com",
+        "dm:bob@zulip.com sender:alice@zulip.com",
+        "dm:bob@zulip.com dm-including:alice@zulip.com",
+        "dm:bob@zulip.com",
     ];
     assert.deepEqual(suggestions.strings, expected);
 
     // Test multiple terms
-    query = "is:starred has:link dm:bob@zulip.com,Smit";
-    suggestions = get_suggestions(query);
+    pill_query = "is:starred has:link dm:bob@zulip.com";
+    query = "Smit";
+    suggestions = get_suggestions(query, pill_query);
     expected = [
-        "is:starred has:link dm:bob@zulip.com,Smit",
+        "is:starred has:link dm:bob@zulip.com Smit",
         "is:starred has:link dm:bob@zulip.com,ted@zulip.com",
+        "is:starred has:link dm:bob@zulip.com sender:ted@zulip.com",
+        "is:starred has:link dm:bob@zulip.com dm-including:ted@zulip.com",
+        "is:starred has:link dm:bob@zulip.com",
         "is:starred has:link",
         "is:starred",
     ];
@@ -377,62 +360,6 @@ test("group_suggestions", ({mock_template}) => {
     suggestions = get_suggestions(query);
     expected = ["has:link dm:invalid@zulip.com,Smit", "has:link"];
     assert.deepEqual(suggestions.strings, expected);
-
-    function message(user_ids, timestamp) {
-        return {
-            type: "private",
-            display_recipient: user_ids.map((id) => ({
-                id,
-            })),
-            timestamp,
-        };
-    }
-
-    direct_message_group_data.process_loaded_messages([
-        message([bob.user_id, ted.user_id], 99),
-        message([bob.user_id, ted.user_id, jeff.user_id], 98),
-    ]);
-
-    // Simulate a past group direct message which should now
-    // prioritize ted over alice
-    query = "dm:bob@zulip.com,";
-    suggestions = get_suggestions(query);
-    expected = [
-        "dm:bob@zulip.com,",
-        "dm:bob@zulip.com,ted@zulip.com",
-        "dm:bob@zulip.com,alice@zulip.com",
-        "dm:bob@zulip.com,jeff@zulip.com",
-    ];
-    assert.deepEqual(suggestions.strings, expected);
-
-    // bob, ted, and jeff are already an existing group direct message,
-    // so prioritize this one
-    query = "dm:bob@zulip.com,ted@zulip.com,";
-    suggestions = get_suggestions(query);
-    expected = [
-        "dm:bob@zulip.com,ted@zulip.com,",
-        "dm:bob@zulip.com,ted@zulip.com,jeff@zulip.com",
-        "dm:bob@zulip.com,ted@zulip.com,alice@zulip.com",
-    ];
-    assert.deepEqual(suggestions.strings, expected);
-
-    // bob, ted, and jeff are already an existing group direct message,
-    // but if we start with just jeff, then don't prioritize ted over
-    // alice because it doesn't complete the full group direct message.
-    query = "dm:jeff@zulip.com,";
-    suggestions = get_suggestions(query);
-    expected = [
-        "dm:jeff@zulip.com,",
-        "dm:jeff@zulip.com,alice@zulip.com",
-        "dm:jeff@zulip.com,bob@zulip.com",
-        "dm:jeff@zulip.com,ted@zulip.com",
-    ];
-    assert.deepEqual(suggestions.strings, expected);
-
-    query = "dm:jeff@zulip.com,ted@zulip.com hi";
-    suggestions = get_suggestions(query);
-    expected = ["dm:jeff@zulip.com,ted@zulip.com hi", "dm:jeff@zulip.com,ted@zulip.com"];
-    assert.deepEqual(suggestions.strings, expected);
 });
 
 test("empty_query_suggestions", () => {
@@ -560,8 +487,8 @@ test("check_is_suggestions", ({override, mock_template}) => {
         "is:alerted",
         "is:unread",
         "is:resolved",
-        "sender:alice@zulip.com",
         "dm:alice@zulip.com",
+        "sender:alice@zulip.com",
         "dm-including:alice@zulip.com",
         "has:image",
     ];
@@ -733,7 +660,7 @@ test("topic_suggestions", ({override, mock_template}) => {
     stream_data.add_sub({stream_id: office_id, name: "office", subscribed: true});
 
     suggestions = get_suggestions("te");
-    expected = ["te", "sender:ted@zulip.com", "dm:ted@zulip.com", "dm-including:ted@zulip.com"];
+    expected = ["te", "dm:ted@zulip.com", "sender:ted@zulip.com", "dm-including:ted@zulip.com"];
     assert.deepEqual(suggestions.strings, expected);
 
     stream_topic_history.add_message({
@@ -751,8 +678,8 @@ test("topic_suggestions", ({override, mock_template}) => {
     suggestions = get_suggestions("te");
     expected = [
         "te",
-        "sender:ted@zulip.com",
         "dm:ted@zulip.com",
+        "sender:ted@zulip.com",
         "dm-including:ted@zulip.com",
         "channel:office topic:team",
         "channel:office topic:test",
@@ -929,10 +856,10 @@ test("people_suggestions", ({override, mock_template}) => {
 
     let expected = [
         "te",
-        "sender:bob@zulip.com",
-        "sender:ted@zulip.com",
         "dm:bob@zulip.com", // bob térry
         "dm:ted@zulip.com",
+        "sender:bob@zulip.com",
+        "sender:ted@zulip.com",
         "dm-including:bob@zulip.com",
         "dm-including:ted@zulip.com",
     ];
@@ -949,12 +876,12 @@ test("people_suggestions", ({override, mock_template}) => {
 
     expected = [
         "te",
-        "sender:bob@zulip.com",
-        "sender:ted@zulip.com",
-        "sender:user299@zulipdev.com",
         "dm:bob@zulip.com",
         "dm:ted@zulip.com",
         "dm:user299@zulipdev.com",
+        "sender:bob@zulip.com",
+        "sender:ted@zulip.com",
+        "sender:user299@zulipdev.com",
         "dm-including:bob@zulip.com",
         "dm-including:ted@zulip.com",
         "dm-including:user299@zulipdev.com",
@@ -1035,7 +962,7 @@ test("people_suggestions", ({override, mock_template}) => {
 
     suggestions = get_suggestions("Ted "); // note space
 
-    expected = ["Ted", "sender:ted@zulip.com", "dm:ted@zulip.com", "dm-including:ted@zulip.com"];
+    expected = ["Ted", "dm:ted@zulip.com", "sender:ted@zulip.com", "dm-including:ted@zulip.com"];
 
     assert.deepEqual(suggestions.strings, expected);